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Research ArticleClinical Studies

Primary Malignant Osseous Neoplasms in the Hand

SHOTA IKE, MASATAKE MATSUOKA, TOMOHIRO ONODERA, ISAO YOKOTA, KOJI IWASAKI, RYOSUKE HISHIMURA, YUKI SUZUKI, EIJI KONDO and NORIMASA IWASAKI
Anticancer Research March 2022, 42 (3) 1635-1640; DOI: https://doi.org/10.21873/anticanres.15639
SHOTA IKE
1Department of Orthopaedic Surgery, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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MASATAKE MATSUOKA
1Department of Orthopaedic Surgery, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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  • For correspondence: masatakem@pop.med.hokudai.ac.jp
TOMOHIRO ONODERA
1Department of Orthopaedic Surgery, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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ISAO YOKOTA
2Department of Biostatistics, Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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KOJI IWASAKI
3Department of Functional Reconstruction for the Knee Joint, Hokkaido University, Sapporo, Japan
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RYOSUKE HISHIMURA
1Department of Orthopaedic Surgery, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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YUKI SUZUKI
1Department of Orthopaedic Surgery, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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EIJI KONDO
4Centre for Sports Medicine, Hokkaido University Hospital, Sapporo, Japan
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NORIMASA IWASAKI
1Department of Orthopaedic Surgery, Faculty of Medicine and Graduate School of Medicine, Hokkaido University, Sapporo, Japan
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Abstract

Background: Primary malignant osseous neoplasms of the hand are rare malignancies. Comprehensive demographic and survival data regarding primary malignant osseous neoplasms of the hand are lacking in the literature. Patients and Methods: Using the Surveillance, Epidemiology, and End Results (SEER) database, we identified all patients with primary malignant osseous neoplasms of the hand diagnosed between 1983 and 2015. Demographic data were searched for primary osseous neoplasms in the hand and higher incidence of histological subtype. Results: A total of 197 patients were analyzed: 103 patients were diagnosed with histologically low-grade tumor, and 31 were diagnosed with high-grade tumor. Five-year cancer-specific and overall survival rates for the entire cohort were 91.4% and 81.9%, respectively. Histological high tumor grade and regional stage from SEER historic stage data were associated with unfavorable cancer-specific survival. Conclusion: Special caution is required if patients have histologically high-grade tumor or tumor extending beyond the periosteum into surrounding joints, as these features worsen cancer-specific mortality.

Key Words:
  • Bone sarcoma
  • SEER program
  • neoplasm grading
  • hand
  • treatment outcome
  • orthopedic surgery

Around 6% of bone tumors develop in the hand (1). Most primary osseous neoplasms in the hand are benign, such as enchondroma, osteochondroma and osteoid osteoma (2-5). Pain, swelling and pathological fractures are relatively common presenting complaints for those pathologies, similar to those for malignant bone tumor (6).

Primary malignant osseous neoplasms of the hand are rare malignancies that develop in the bones of the hand, accounting for less than 1% of all primary malignant osseous neoplasms (7). Due to this rarity, few intensive centers accumulate extensive experience in the treatment of patients with these lesions, and general orthopedic surgeons rarely encounter patients with sarcomas of the hand bones. Unfortunately, this can delay suspicion of clinical malignancy and thus contribute to significantly delayed diagnosis (8).

Most patients with bone tumors in the hand visit orthopedic clinics, where they are commonly examined by an orthopedic surgeon. All orthopedic surgeons therefore need to understand the clinicopathological features of primary malignant osseous neoplasms of the hand to be able to distinguish benign tumors from life-threatening tumors. However, comprehensive demographic and survival data regarding primary malignant osseous neoplasms of the hand are lacking in the literature.

Considering the rarity of primary malignant osseous neoplasms of the hand, information from a large number of patients is required. We hypothesized that a nationwide oncology registry would contain clarifying data for primary malignant osseous neoplasms of the hand. The purposes of the current study were to: i) Clarify the demographic features of primary malignant osseous neoplasms of the hand; and ii) identify factors associated with survivability.

Patients and Methods

Patient information was obtained using the Surveillance, Epidemiology, and End Results (SEER) database that collects cancer incidence data from population-based cancer registries covering approximately 28% of the United States population. The following inclusion criteria were used: i) International Classification of Diseases for Oncology (ICD-O) code C40.1 (short bones of the upper limb and associated joints); ii) diagnosis between 1983 and 2015; and iii) diagnosis with histological confirmation from either biopsy or surgical pathology. Exclusion criteria were as follows: Hematological malignancy; glioma-related cancer; soft-tissue tumor; or unknown histology or cause of death. Data extracted from the SEER database included patient demographics, stage at diagnosis, tumor grade, tumor type, cause of death, surgical treatment, SEER historic stage (localized: no sign that the cancer had spread outside of the bone in which it started; regional: tumor growth outside the bone and into nearby bones or other structures, or tumor extending into regional lymph nodes by way of the lymphatic system; distant: tumor spread to distant parts of the body), and survival time. As SEER employs an original histological grading system, we defined SEER grades 1 and 2 as low-grade tumor, and grades 3 and 4 as high-grade tumor. SEER *Stat software (version 8.3.8; National Cancer Institute, Bethesda, MD, USA) was used to obtain information from the SEER database.

All anonymized data used in this study were obtained from the SEER database. An individual SEER ID was used to support our analysis. Ethical review and approval was not required for this study on human participants, in accordance with local legislation and institutional requirements. All procedures in this study involving human participants were performed in accordance with the ethical standards of the 1964 Declaration of Helsinki and its later amendments. A comprehensive agreement for academic use of information such as type of treatments, treatment progress or any other data acquired during their treatments was obtained from the patients by the hospital at the time of their hospitalization, and no identifying information of the participants is included in this article.

The primary outcome of this study was to report the demographic data for primary malignant osseous neoplasms of the hand. Cancer-specific survival (CSS) was defined as the duration from the date of diagnosis until death due to cancer and overall survival (OS) was defined as the duration from date of diagnosis to death or last follow-up, with no restriction on cause of death. CSS and OS were calculated by Kaplan–Meier survival analyses. The secondary outcome was to report risk factors affecting survival in patients with primary malignant osseous neoplasms of the hand. Survival analyses were performed by Cox proportional hazards modeling to evaluate six predictor variables (age, gender, laterality, histological grade, SEER historic stage and chemotherapy). Because only 15 CSS events were identified (160 patients survived), additional analyses were performed using only two predictor variables (histological grade and SEER historic stage) to confirm the results. All data were analyzed using JMP Pro version 16.0.0 statistical software (SAS Institute, Cary, NC, USA).

Results

Following the inclusion criteria, a total of 222 patients with primary malignant osseous neoplasms of the hand diagnosed between 1983 and 2015 were collected from the SEER database. After applying exclusion criteria, 194 patients were enrolled in this study (Figure 1). The details of patient characteristics are described in Table I. The median age at diagnosis was 52 years.

Figure 1.
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Figure 1.

Flowchart showing the process of including patients in this cohort. COD: Cause of death.

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Table I.

Baseline characteristics of patients with malignant primary osseous neoplasm of the hand at diagnosis (n=194).

Of the 194 patients with primary malignant osseous neoplasms of the hand, most were male (45%) and White (85%). A total of 103 patients (53%) were diagnosed with histologically low-grade tumor, 30 (15%) with high-grade tumor, and 61 (31%) with unknown histological grade. Among these patients, 54 (28%) had undergone limb amputation and 104 (54%) resection. Surgical management was defined at the time of care according to the treatment provided, and the SEER registry does not differentiate between intra-lesional resection and wide resection with tumor-free margins. A total of 47 patients (24%) received chemotherapy and 13 (7%) received radiotherapy. Based on SEER historic stage, 96 cases (49%) were localized, 76 (39%) were regional, eight (4%) were distant and 14 (7%) were unstaged.

Next, we examined associations between specific histological subtypes and primary malignant osseous neoplasms of the hand according to the World Health Organization classification of tumors (fifth edition) (9). The most common histological subtypes were central chondrosarcoma, grades 2 and 3 (55%), osteosarcoma (16%), and Ewing sarcoma (11%) (Table II).

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Table II.

Histological type according to the World Health Organization classification of tumors (fifth edition) (9).

Five- and 10-year CSS rates for the entire cohort with primary malignant osseous neoplasm of the hand were 92% and 91%, respectively. Five- and 10-year OS rates were 83% and 71%, respectively. In subclass analyses according to SEER historic stage (Figure 2), 5-year CSS and OS rates in patients with localized stage were 97% and 94%, respectively. Five-year CSS and OS rates in patients with regional stage were 88% and 73%, respectively. Five-year CSS and OS rates in patients with distant stage were 70% and 70%, respectively. For unstaged patients, 5-year CSS and OS rates were 79% and 66%, respectively. According to histological grade (Figure 3), 5-year CSS and OS rates of patients with high-grade tumor were 80% and 78%, respectively. For patients who had low-grade tumors, CSS and OS rates were 97% and 85%, respectively. CSS and OS rates of patients with unknown tumor grade were 89% and 82%, respectively.

Figure 2.
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Figure 2.

Kaplan–Meier curves for cancer-specific (A) and overall (B) survival rates according to Surveillance, Epidemiology, and End Results (SEER) historic stage for the cohort.

Figure 3.
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Figure 3.

Kaplan–Meier curves for cancer-specific (A) and overall (B) survival according to histological grade for the cohort.

Finally, we investigated risk factors associated with survival. After excluding those with distant and unstaged lesions according to SEER historic stage due to the limited numbers of patients, Cox proportional hazard modeling was applied with factors of age, gender, laterality, SEER historic stage, histological grade, and status of chemotherapy (Table III). Histological high-grade tumor shortened CSS [hazard ratio (HR)=8.07, 95% confidence interval (CI)=1.63-39.90, p=0.01] but not OS (HR=1.50, 95% CI=0.66-3.43, p=0.33). In addition, regional SEER historic stage shortened both CSS (HR=3.98, 95% CI=1.15-13.71, p=0.03) and OS (HR=1.98, 95% CI=1.12-3.50, p=0.02). Considering the low number of CSS events, we performed additional analyses using two predictor variables, namely histological grade and SEER historic stage. Similarly to the earlier results, high histological tumor grade shortened CSS (HR=7.49, 95% CI=1.87-29.99, p<0.01) but not OS (HR=1.02, 95% CI=0.47-2.23, p=0.95). In addition, regional SEER historic stage shortened CSS and OS (CSS: HR=3.36, 95% CI=1.06-10.68, p=0.04; OS: HR=2.22, 95% CI=1.28-3.86, p<0.01).

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Table III.

Cox proportional hazard model with factors of age, sex, laterality, Surveillance, Epidemiology, and End Results (SEER) historic stage, histological grade, and status of chemotherapy.

Discussion

Primary malignant osseous neoplasms of the hand are rare. We therefore employed the SEER database to clarify conditions for primary malignant osseous neoplasms of the hand. To the best of our knowledge, this study represents the first report of comprehensive demographic and survival data regarding primary malignant osseous neoplasms of the hand. Data from this study clearly demonstrated that: i) Survival of patients with primary malignant osseous neoplasms of the hand was relatively favorable; ii) histologically high-grade tumor was associated with worsened CSS, and regional SEER historic stage was associated with worsened CSS and OS. Tumor spread via the lymphatic system is highly unusual in malignant bone sarcoma (10, 11), so direct invasion into surrounding tissues might have a much greater impact on survival. Our study using a population-based cancer database provided new insights into primary malignant osseous neoplasms of the hand.

The objectives of surgery for bone sarcoma are to achieve both maximal resection for oncological control and conservation of function. Amputation surgery can be devastating for patients but is sometimes required to achieve adequate oncological margins. Because of advanced multimodal treatments such as radiotherapy, chemotherapy and reconstruction techniques, no more than 10% of patients with sarcoma undergo amputation (12-14). In the current study, the amputation rate for primary malignant osseous neoplasms of the hand was higher than previously reported (12-15). Limited soft-tissue coverage is a common problem for defects of the hand (16), which may have contributed to the high amputation rate in our study, although multiple options for free tissue transfer and other soft-tissue coverage options permit salvage of the hand, even if partial.

According to SEER historic stage (7), 5-year CSS rates in chondrosarcoma are 87% in patients with localized tumors and 83% in those with regional tumors, while 5-year CSS rates in osteosarcoma are 74% in those with localized tumors and 66% in those with regional tumors. In addition, 5-year CSS rates in Ewing sarcoma are 82% in patients with localized tumors and 67% in those with regional tumors, while in patients with malignant giant-cell tumor of bone, it is 79% for all stages. In our cohort, the 5-year CSS for primary malignant osseous neoplasms of the hand overall was relatively favorable compared to those for other sites of development. Improved survival rates for sarcoma, including soft-tissue sarcoma of the hand, have been reported from single-institution experiences (17). Hand lesions tend to become symptomatic and thus are diagnosed earlier due to limited soft-tissue coverage, resulting in these tumors tending to be diagnosed at a smaller size and earlier stage (18, 19).

Although bone sarcoma is rare, descriptive epidemiological studies using large cancer databases are increasingly revealing prognostic factors for patients with bone sarcoma. Akiyama et al. investigated the Bone and Soft Tissue Tumor Registry of Japan and identified older age (≥65 years) as a poor prognostic factor regardless of histological subtype (20). Bohman et al. investigated patients with skull base chondrosarcoma using the SEER database and demonstrated that earlier decade of diagnosis, increased age, and mesenchymal chondrosarcoma were associated with reduced survival (21). Zhang et al. investigated the SEER database to seek prognostic factors for overall primary sarcoma and reported factors including older age, high-grade tumor, regional and distant SEER historic stage, development in the extremities, larger tumor (diameter ≥8 cm), and patients without surgical intervention (22). In the current study, regional SEER historic stage and histologically high-grade tumor were associated with unfavorable CSS, although histological subtypes were not considered due to the limited number of patients in our cohort. In addition, we did not detect prognostic factors associated with OS, probably because of the lack of information regarding comorbid conditions or details of patient background.

Several issues should be considered when interpreting our results. Firstly, our data were from population-based cancer registries of the United States population. The SEER database includes a high rate of cases of unknown histological grade and does not provide information regarding Eastern Cooperative Oncology Group performance status, surgical stage, details of treatment for each patient, or surgical margins, all of which could contribute significant bias. Caution is therefore needed when interpreting our results because we were unable to take into account Eastern Cooperative Oncology Group performance status or treatment details that could lead to significant bias. On the other hand, considering that bone sarcoma comprises a variety of histological subtypes with limited numbers of patients for each, a large, population-based cohort is useful to address the demographic and survival characteristics of patients with bone sarcoma. Future randomized clinical research including data missing from the SEER database is needed to confirm our results. Secondly, the SEER database did not distinguish between primary, secondary, or post-radiation tumors in terms of malignant giant-cell tumor of bone. The histological features and prognosis are known to differ between primary and secondary malignant giant-cell tumor (23-25). These factors might therefore affect survival. Finally, we did not consider functional reconstruction, although this represents a critical factor for optimizing the outcome of hand surgery (13, 16). The amputation rate in the current cohort was around 30%, suggesting unfavorable functional outcomes for patients with primary malignant osseous neoplasms of the hand. Further research to clarify functional outcomes is needed. Nevertheless, using the SEER database, this study provides important insights into these rare malignancies of the hand.

Conclusion

Our study using a large cancer database provided new insights about primary malignant osseous neoplasms of the hand. Although relatively favorable survival rates can be expected in patients with sarcomas of the hand bones, special caution is required for patients with histologically high-grade tumor or tumor that extends beyond the periosteum into surrounding joints, as these factors are associated with worse CSS rates.

Footnotes

  • Authors’ Contributions

    MM was involved in the design of the study; performed clinical assessments, analyses, and interpretation of data; and drafted and revised the article. SI, TO, IY, KI, RH and YS assisted with data interpretation and revised the article for important intellectual content. EK and NI were involved in data acquisition and critically revised the article for important intellectual content. All Authors have read and approved the final article.

  • Conflicts of Interest

    None declared.

  • Received December 22, 2021.
  • Revision received January 17, 2022.
  • Accepted January 20, 2022.
  • Copyright © 2022 International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved.

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Anticancer Research: 42 (3)
Anticancer Research
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March 2022
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Primary Malignant Osseous Neoplasms in the Hand
SHOTA IKE, MASATAKE MATSUOKA, TOMOHIRO ONODERA, ISAO YOKOTA, KOJI IWASAKI, RYOSUKE HISHIMURA, YUKI SUZUKI, EIJI KONDO, NORIMASA IWASAKI
Anticancer Research Mar 2022, 42 (3) 1635-1640; DOI: 10.21873/anticanres.15639

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Primary Malignant Osseous Neoplasms in the Hand
SHOTA IKE, MASATAKE MATSUOKA, TOMOHIRO ONODERA, ISAO YOKOTA, KOJI IWASAKI, RYOSUKE HISHIMURA, YUKI SUZUKI, EIJI KONDO, NORIMASA IWASAKI
Anticancer Research Mar 2022, 42 (3) 1635-1640; DOI: 10.21873/anticanres.15639
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Keywords

  • Bone sarcoma
  • SEER program
  • neoplasm grading
  • hand
  • treatment outcome
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