Radiation-induced carcinoma of the lung— the St. Lawrence tragedy

Volume 74,

Number 4

The Journal of

October 1977

THORACIC AND

CARDIOVASCULAR SURGERY

Radiation-induced carcinoma of the lungthe St. Lawrence tragedy This paper reviews the problem of radiation-induced carcinoma of the lung in the fluorspar mines of Newfoundland. Seventy-eight workers have died from this disease since commercial operation commenced in 1933. In 1959 the source of the radiation was identified as radon, and its daughter nucleotides present as contaminants in water seeping into the mines. Heavy smoking is probably a synergistic cocarcinogen. The histology in this group of patients with radiation-induced lung cancers is unusual, since squamous cell carcinoma accounts for 90 percent of all cases. There have been four patients with second primary lung cancers. Radical radiotherapy has been the primary mode of treatment based on the reluctance of the miners to undergo operation. Surprisingly good results have been obtained, with an average survival time of 34 months after treatment. Institution of improved ventilation has reduced radiation to safe levels, but an estimated 120 miners from the pre-1960 era are still at risk.

Earle S. Wright, M.D. (by invitation), and Cecil M. Couves, M.D., St. John's, Newfoundland, Canada

In 1897 Hartung and Hesse identified a malignant disease of the lung as the mysterious ailment responsible for the high death rate in the pitchblende miners of Schneeberg, Saxony. Uhlig, in In I , related the incidence of this lesion to high levels of radiation in the mines. The story of Joachimsthal in Czechoslovakia is similar. Although a high mortality rate was noted in miners from its foundation in 1516, only in 1926 was it From the Department of Surgery, Memorial University of Newfoundland, SI. John's, Newfoundland, Canada. Read at the Fifty-seventh Annual Meeting of The American Association for Thoracic Surgery, Toronto, Ontario, Canada, April 18, 19, and 20, 1977. Address for reprints: Earle S. Wright, M.D., Department of Surgery, Memorial University of Newfoundland, SI. John's, Newfoundland, Canada AIC 5S7.

realized that the cause of death was identical to that in Schneeberg. The death rate from bronchogenic carcinoma in miners at both sites was approximately 50 percent.' In spite of these studies, public health authorities throughout the world appeared to be unaware of the dangers of radiation in underground mines. St. Lawrence is a small coastal community in Southern Newfoundland (Fig. I). Its economy is based entirely on fishing and the mining of fluorspar. This mineral, calcium fluoride, is widely used in the manufacture of aluminum and steel and, to a lesser degree, in the spray-propellant industry. In a survey of the south coast of Newfoundland in 1765, Captain James Cook recorded a "blue beach" in St. Lawrence harbor, presumably the result of an outcropping of fluorspar. In 1843 an English geologist, Jukes, noted the occurrence 495

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The Journal of Thoracic and Cardiovascular Surgery

Wright and Couves

S1. JOHN'S

Fig. 1. Map of the province of Newfoundland showing location of St. Lawrence.

Table I. Decay products of uranium Uranium

~ Thorium ~ Radium ~ Radon ~ Radon daughters

A, B, C, ~

c-

Polonium

~

Lead of fluorite in the St. Lawrence area, and this was confirmed in a more extensive survey by Murray and Howley in 1870. The first fluorspar mines commenced commercial operation in 1933.

Recognition and investigation of the "St. Lawrence problem" In 1949 the first miner died of carcinoma of the lung. By 1954 an additional eight deaths from this disease had occurred, and it was obvious that a serious problem

existed. In 1956 the Department of National Health and Welfare began an epidemiologic and clinical investigation. It was not until 1959, however, that a radiation survey revealed levels of radioactivity far in excess of permissible working levels. In some areas concentrations of up to 193 times the recommended limit were found. The responsible agents were radon gas and its short-lived daughter nucleotides. The exact source of these materials never has been located, despite intensive investigations. Since radon222 could be derived only from the breakdown of uranium (Table I), the search concentrated on a source of the element. No significant amounts of uranium were found, but excessive amounts of radon were discovered in the water seeping into the mines. Expert opinion supports the theory that this water has become contaminated by a leaching action on uranium contained in the granite rocks surrounding the mines.

Incidence To date 78 miners have died of carcinoma of the lung. This figure represents approximately 36 percent of the population at risk. The majority of these individuals have had underground experience exceeding IO years. In one case, however, total exposure was only

Volume 74

Radiation-induced carcinoma of lung

Number 4

49 7

October, 1977

Table II. Sputum cytology studies in lung cancer in St. Lawrence miners No. of patients

26

Squamous cell carcinoma (keratinizing type-8) Oat-cell carcinoma Adenocarcinoma

2

e >

vi

<.:l

700

(.)

e >

600

vi <:)

(.)

I

Total

29

VI

IX

400

Table III. Relative distribution of histologic types of lung cancer in control subjects. United States uranium miners. and St. Lawrence fluorspar miners Squamous cell

Undifferentiated small cell

Adenocarcinoma and others

200

59 25

14 64

27 II

100

90

7

3

I Control subjects U. S. uranium miners S1. Lawrence miners

300

1,600 hours. Only three cases of the disease have been reported in nonminers in the community over the same period. The incidence of lung cancer in the St. Lawrence miners is estimated at 29 times the provincial rate for men of a comparable age group.

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~( LUNG CANCER CASES - NO. OF DEATHS/loo,ooo POPULATION/YEAR (SACCOMANOI

Fig. 2. Incidence of lung cancer in smoking and nonsmoking miners. Calculated on number of deaths per 100,000 population per year (provided by G. Saccomanno).

There is abundant evidence to show that smoking is a potent cocarcinogen in cases of radiation carcinoma of the lung. Saccomanno" found an incidence of four per 100,000 population per year in nonsmoking uranium miners as compared with 700 per 100,000 population per year in uranium miners who smoked. Saccomanno also noted that in nonuranium miners the incidence of lung carcinoma was directly related to the number of cigarettes consumed (Fig. 2). There were only two nonsmokers among the 78 miners who died with lung cancer. A 1960 survey showed that only 5 percent of the miners then employed were nonsmokers. The average consumption was in excess of 30 cigarettes per day. The synergistic effect of smoking may be based on a delayed elimination of carcinogens by paralysis of ciliary action.

cinoma, undifferentiated small cell carcinoma, and adenocarcinoma was increased. However, the greatest increase was noted in undifferentiated small cell tumors, for they accounted for almost two thirds of lung cancers in this group. In a later study Archer, Saccomanno, and Jones" showed that the absolute frequency of the different histologic types was dose dependent. However, the relative frequency was independent of the degree of radiation exposure. In marked contrast the overwhelming majority of the lung cancers in the St. Lawrence miners have been epidermoid (Tables II and III). There is no obvious explanation for this disparity. Second primary lung cancers have occurred in four patients. This is not surprising, since pathologic studies strongly suggest the multicentric origin of bronchogenic carcinoma. Auerbach and associates" found areas of carcinoma in situ in the lungs of 77 percent of patients dying with lung cancer. The relative rarity of multiple primary lung tumors may be related to the short life span of most patients with this lesion.

Pathology

Treatment

Saccomanno and co-workers," in a study of the histologic types of lung carcinoma in uranium miners, concluded that the incidence of squamous cell car-

The primary method of treatment has been radiotherapy (Table IV). This is due to reluctance of the miners to undergo surgical resection. The short sur-

Role of smoking as a cocarcinogen

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The Journal of Thoracic and Cardiovascular Surgery

Wright and Couves

Table IV. Results of treatment Range

Survival average

No.

(mo.)

(mo.)

alive

2 to 4 2 mo. to 9'12 yr.

3 34

2 to 8

5'/2

No.

Surgical resection Radical radiation Palliative radiation Palliative radiation plus chemotherapy No treatment

5 15

Nil

2 for 6 yr. I for 7 yr.

5 5

5 to IO

7

Nil Nil

6

3 to 27

IO

Nil

vival period following resection in a few early cases led to the widespread belief that exposure of the cancer to the air accelerated its growth rate. This series is unique, therefore, in that a group of patients with lung cancer have been treated with radiotherapy without any prior selection. Radical radiotherapy has yielded surprisingly good results. The average survival period after treatment in a group of 15 patients has been 34 months. Two patients are still alive at 6 and 7 years, and a third died from a myocardial infarct 9% years after radiotherapy. In the Colorado plateau uranium miners, the median time from diagnosis to death was only 2 months." This striking difference in the survival times of the two groups clearly is related to the predominant histologic typeundifferentiated small cell in the uranium miners as opposed to epidermoid in the St. Lawrence group.

One can only hope that this industrial disaster is the final story in the tragic history of radiation-induced carcinoma of the lung.

The present situation

3 Saccomanno, G. C., Archer, V. E., Auerbach, 0., Kuschner, M., Saunders, R. P., and Klein, M. G.: Histologic Types of Lung Cancer Among Uranium Miners, Cancer 27: 515, 1971. 4 Archer, V. E. Saccomanno, G., and Jones, J. H.: Frequency of Different Histologic Types of Bronchogenic Carcinoma as Related to Radiation Exposure, Cancer 34:

Following the discovery of excessive radiation in the mines in 1959, improved ventilation was installed promptly. This reduced the radioactivity to well below suggested working levels. In addition, each miner now has his exposure monitored by methods similar to those employed for workers in x-ray departments. In the meantime, however, new cases inexorably continue to appear among the pre-1960 miners. It is estimated that approximate!y 120 men are still at risk. The story of St. Lawrence has been described poignantly by the Newfoundland anthropologist, Elliot Leyton, 7 in a book appropriately titled Dying Hard. In the first chapter Leyton states: "One household in every three has a dead or dying miner in the towns of St. Lawrence and Lawn. There is no family that has not been numbed by the loss of a father, an uncle, a son or a brother. Many have lost several."

We gratefully acknowledge the assistance of the following individuals who permitted access to their files: Dr. K. Hong, Department of Radiotherapy, General Hospital, St. John's, Dr. D. Parsons, Department of Medicine, General Hospital, St. John's, and Dr. B. Hollywood, St. Lawrence Memorial Hospital, St. Lawrence. REFERENCES Hueper, W. C.: Occupational Tumours and Related Diseases, Springfield, Ill., 1942, Charles C Thomas, Publisher, p. 435. 2 Saccomanno, G. C.: Report of Royal Commission, Respecting Radiation, Compensation and Safety at the Fluorspar Mines, St. Lawrence, Newfoundland, Canada, 1969, p. 108.

2056, 1974.

5 Auerbach, 0., Gere, J. B., Pawlowski, 1. M., Muehsam, G. E., Smolin, H. J., and Stout, A. P.: Carcinoma-in-Situ and Early Invasive Carcinoma Occurring in the Tracheobronchial Trees in Cases of Bronchial Carcinoma, J. THORAc. SURG. 34: 298, 1957. 6 Saccomanno, G. c., Archer, V. E., Saunders, R. P., James, L.A., and Beckler, P. A.: Lung Cancer of Uranium Miners on the Colorado Plateau, Health Phys. 10: 1195, 1964. 7 Leyton, E. Dying Hard, Toronto, 1975, McClelland and

Stewart, p.ll.