Primary Care Physician Supply and Colorectal Cancer

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Primary Care Physician Supply and Colorectal Cancer

OBJECTIVE: Our goal was to determine if increasing primary care physician supply was associated with lower incidence and mortality rates for colorectal cancer.

STUDY DESIGN: We performed an ecologic study of Florida’s 67 counties, using data from the state tumor registry and the American Medical Association physician masterfile.

POPULATION: Florida residents were included.

OUTCOMES MEASURED: We measured age-adjusted colorectal cancer incidence and mortality rates for Florida’s 67 counties during the period 1993 to 1995.

RESULTS: Increasing primary care physician supply was negatively correlated with both colorectal cancer (CC) incidence (CC = -0.46; P < .001) and mortality rates (CC = -0.29; P =.02). In linear regression that controlled for other county characteristics, each 1% increase in the proportion of county physicians who were in primary care specialties was associated with a corresponding reduction in colorectal cancer incidence of 0.25 cases per 100,000 (P < .001) and a reduction in colorectal cancer mortality of 0.08 cases per 100,000 (P=.008).

CONCLUSIONS: Incidence and mortality of colorectal cancer decreased in Florida counties that had an increased supply of primary care physicians. This suggests that a balanced work force may achieve better health outcomes.

It was predicted that more than 130,000 Americans would develop colorectal cancer in the year 2000. This is the second leading cause of cancer mortality in the United States, with an estimated 56,300 deaths predicted for 2000.1 In that year, the state of Florida ranked third in the number of colorectal cancer cases (9100) and colorectal cancer deaths (3900).

Earlier diagnosis of colorectal cancer, with subsequently reduced mortality, can be achieved by eliciting and promptly evaluating signs and symptoms of colorectal cancer and by providing recommended screening tests, such as fecal occult blood testing and flexible sigmoidoscopy.2 Also, the provision of screening tests may reduce colorectal cancer incidence by detecting and eliminating precancerous polyps. Annual fecal occult blood testing, for example, has been demonstrated to reduce colorectal cancer incidence by 20%.3 Polyps found by screening sigmoidoscopy would also generally result in surveillance colonoscopy, a procedure which may reduce colorectal cancer incidence by as much as 90%.4

Studies have consistently reported that access to health care and a physician’s recommendation for screening are important predictors of cancer screening.5-10 One would expect, therefore, that the provision of colorectal cancer screening tests would be dependent to some extent on the availability of physician services. Physician specialties may differ, however, in their provision of preventive health services. Stange and colleagues,11 for example, found that family physicians addressed at least one US Preventive Services Task Force recommendation for preventive care in 39% of visits for chronic illness. In contrast, evidence suggests that most specialists are not likely to address health care needs outside their specialty.12

Compared with other cancer screening tests, colorectal cancer screening is less frequently recommended by physicians and is less frequently completed by patients. It is possible, therefore, that the availability of primary care providers has relatively limited impact on colorectal cancer outcomes.13-15 We have previously shown that increasing supplies of primary care physicians were associated with earlier detection of colorectal cancer, while increasing supplies of non–primary care physicians were associated with later-stage diagnosis.16 We hypothesized, therefore, that increasing primary care physician supply would also be associated with lower incidence and mortality rates for colorectal cancer.

Methods

We performed an ecologic study comparing primary care physician supply with colorectal cancer incidence and mortality rates. Colorectal cancer incidence and mortality rates for Florida’s 67 counties were identified using the Florida Cancer Data System (FCDS), a population-based statewide cancer registry. The FCDS is a member of the North American Association of Central Cancer Registries (NAACCR). NAACCR audits have estimated that the completeness of case ascertainment for the period 1990 to 1994 is 99.7%. The FCDS provides age-adjusted incidence and mortality rates by standardizing them to the 1970 US standard population. To account for year-to-year fluctuations, rates were averaged over the 3-year period 1993 to 1995.

Because distal cancers may be more easily detected with screening tests such as sigmoidoscopy, we also examined incidence rates stratified by proximal versus distal origin of the cancer. We defined proximal cancers as those arising from the cecum, ascending colon, hepatic flexure, transverse colon, and splenic flexure. Distal cancers were defined as those arising from the descending colon, sigmoid colon, rectosigmoid juncture, and the rectum. Tumors of the anal canal were excluded because of differing pathology and treatment implications.17

We used the 1990 US census to ascertain other characteristics of Florida counties that might have an impact on colorectal cancer incidence and mortality. In addition to age, colorectal cancer incidence and mortality rates vary by race, socioeconomic status, and marital status. Variables obtained for each county included median household income, percentage of county residents with less than a high school education, percentage residing in urban census areas, percentage who were white, and percentage who were married.

 

 

Data on physician supply were obtained from the 1994 American Medical Association (AMA) physician masterfile, which includes allopathic and osteopathic physicians regardless of AMA membership. County-level population estimates were obtained from the 1990 United States Census. Physician supply variables were created for total physician supply, and for primary care physician supply and non–primary care physician supply. Physicians were classified as primary care if their self-designated specialty was family practice, general practice, obstetrics/gynecology, or general internal medicine.

Physicians who indicated they were engaged in full-time direct patient care were counted as one full-time equivalent (FTE); those who indicated in the masterfile that they were either “semi-retired,” in residency training, or engaged in teaching or research were counted as 0.5 FTE. Physicians who indicated they were no longer involved in direct patient care were excluded. On the basis of this information, we calculated for each county the proportion of all physicians engaged in primary care and used this as our measure of primary care supply.

Counties were the unit of analysis for our study. We explored associations between primary care physician supply, and colorectal cancer incidence and mortality rates in 2 ways. First we constructed scatterplots to explore possible linear relationships, and to exclude nonlinear associations, and also calculated Pearson correlation coefficients. Second, we used multiple linear regression to explore the multivariable relationship between primary care physician supply and outcomes, controlling for other county-level characteristics.

Parameter estimates were determined using the method of ordinary least squares. Potential confounding variables included in each initial model were median household income, percentage of county residents with less than a high school education, percentage residing in urban census areas, percentage who were white, percentage who were married, and total physician supply. Final regression models included all variables that remained statistically significant (P < .05), using a backward variable selection algorithm. We also confirmed that all outcomes were normally distributed using graphical methods.

Results

The average physician supply for Florida’s 67 counties (physicians per 100,000 population) was 134.9, with primary care supply at 49.7 and specialist supply at 85.2. The average supply of primary care specialties was as follows: family physicians, 17.5; general practitioners, 10.7; general internists, 13.9; and obstetrician-gynecologists, 7.2. There was substantial variation in physician supply, with some counties having as few as 15 physicians per 100,000 population and other counties having more than 500 physicians per 100,000 population. The average proportion of physicians who were in a primary care specialty was 0.36 across Florida’s 67 counties (standard deviation = 0.19; range = 0.17-1.00).

There was also substantial variation in both incidence and mortality rates across Florida’s 67 counties. Some counties had incidence rates as low as 9.6 cases per 100,000 and others as high as 72 cases per 100,000. Mortality rates varied from a low of 3.8 cases per 100,000 to a high of 26.4 cases per 100,000. Incidence and mortality rates were both higher in men than in women.

Associations between primary care physician supply and colorectal cancer incidence and mortality rates were assessed both graphically and using the Pearson correlation coefficient Table 1.* ( Figure 1, Figure 2, Figure 3) Primary care physician supply was negatively correlated with colorectal cancer incidence and mortality rates in the 67 counties studied. For colorectal cancer incidence rates, negative correlations were observed for both proximal and distal cancers, and among both men and women. For mortality rates, correlations were stronger for men and did not reach statistical significance among women. Scatter diagrams did not suggest the presence of nonlinear relationships.

Table 2 presents the results of linear regression analyses. Primary care physician supply was a statistically significant predictor of all outcomes examined. Each 1% increase in primary care physician supply was associated with a reduction in overall colorectal cancer incidence of 0.25 cases per 100,000. Each 1% increase in primary care physician supply was similarly associated with a reduction in overall colorectal cancer mortality of 0.08 cases per 100,000. In stratified analysis, primary care physician supply had similar effects for both proximal and distal cancers, with slightly greater effects among men than women. Overall physician supply was not a significant predictor of any of the outcomes examined.

Discussion

We found that an increasing supply of primary care physicians was associated with lower incidence and lower mortality rates of colorectal cancer in Florida counties. Each 1% increase in primary care physician supply was associated with a reduction in colorectal cancer incidence of 0.25 cases per 100,000 and a reduction in mortality of 0.08 cases per 100,000. In contrast, overall physician supply was unrelated to any of the outcomes examined. Findings were similar in men and women and for proximal and distal cancers.

 

 

Although there is continued interest in the composition of the United States physician work force,18-25 there have been surprisingly few studies demonstrating the effects of physician supply on health-related outcomes. Some studies have suggested that an oversupply of specialists may contribute to higher health care costs.22,26-28 Primary care physician supply has been correlated with reduced hospitalization rates for ambulatory care–sensitive conditions29,30 and with improved access and overall use of ambulatory health services.31-34

We have previously shown associations between primary care physician supply and earlier detection of breast cancer, colorectal cancer, and malignant melanoma.16,35,36 These findings are consistent with studies showing that patients who have a family physician are more likely to receive a diagnosis of early-stage cancer.37 Our study suggests that increasing supplies of primary care physicians might also be associated with reduced incidence and mortality for some cancers. In contrast, increased overall supplies of physicians have not been associated with improved cancer outcomes, suggesting that a balanced physician work force may be necessary to achieve optimal health outcomes.

Physician specialty choice and practice location are driven by many factors, including the location of training programs at medical schools and residencies, role models in medical school, education debt, lifestyle, and other issues. These factors influence the types of physicians that practice in various locations, and as a result may influence the health care of the population in that area. As the physician work force is studied and policy decisions are made, it will be important to consider measurable health care outcomes in addition to projected demands based on economic forces.38

Limitations

This study has a number of important limitations that should be considered. First, ecologic studies are subject to the ecologic fallacy, in which associations at the population level do not accurately reflect associations at the individual level. We did not have information on individual patients’ actual use of physician services, for example, so patients’ actual access to primary care may have been different than that predicted by county-level measures. Ecologic studies have very limited ability to establish causation, and follow-up studies conducted at the individual patient level (such as case-control or cohort studies) will be necessary to confirm these findings. The exploratory nature of selecting variables for ecologic studies may also increase type 1 statistical errors, falsely concluding that associations exist when they have actually occurred by chance.

We did not have information on other colorectal cancer risk factors, such as dietary patterns, rates of family history, or rates of ulcerative colitis. We also lacked information on rates of detection of precancerous polyps, and the age/sex distribution of physicians, which would have strengthened our study. Because incidence and mortality rates were established according to the patient’s county of residence rather than the location of diagnosis or treatment, we do not believe the associations observed were the result of referral patterns (eg, patients with suspected late-stage disease being referred to areas with higher-specialty physician supply). However, physician supply might be correlated with other unmeasured characteristics of our health care delivery system, which could account for the observed associations. Finally, our study was restricted to colorectal cancer in Florida, which may not be representative of other diseases or other parts of the country.

Conclusions

Both the incidence and mortality of colorectal cancer were decreased in Florida counties that had a greater supply of primary care physicians. Overall physician supply, however, was unrelated to colorectal cancer mortality or incidence. These associations will need to be confirmed with studies conducted at the individual level.

References

1. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000;50:7-33.

2. United States Preventive Service Task Force. Guide to clinical preventive services. 2nd ed. Washington, DC: US Department of Health and Human Services; 1996.

3. Mandel JS, Church TR, Bond JH, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med 2000;343:1603-07.

4. Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal cancer by colonoscopic polypectomy: The National Polyp Study Workgroup. N Engl J Med 1993;329:1977-81.

5. Fox SA, Murata PJ, Stein JA. The impact of physician compliance on screening mammography for older women. Arch Intern Med 1991;151:50-56.

6. Fox SA, Siu AL, Stein JA. The importance of physician communication on breast cancer screening of older women. Arch Intern Med 1994;154:2058-68.

7. Breen N, Kessler L. Changes in the use of screening mammography: evidence from the 1987 and 1990 National Health Interview Surveys. Am J Public Health 1994;84:62-67.

8. National Cancer Institute Breast Cancer Screening Consortium. Screening mammography: a missed clinical opportunity? JAMA 1990;264:54-58.

9. Lewis SF, Jensen NM. Screening sigmoidoscopy: factors associated with utilization. J Gen Intern Med 1996;11:542-44.

10. Vernon S. Participation in colorectal cancer screening: a review. J Natl Cancer Inst 1997;89:1406-22.

11. Stange K, Flocke S, Goodwin M. Opportunistic preventive services delivery. J Fam Pract 1998;46:419-24.

12. Rosenblatt RA, Hart LG, Baldwin LM, Chan L, Schneeweiss R. The generalist role of specialty physicians: is there a hidden system of primary care? JAMA 1998;279:1364-70.

13. Brownson RC, Davis JR, Simms SG, Kern TG, Harmon RG. Cancer control knowledge and priorities among primary care physicians. J Cancer Educ 1993;8:35-41.

14. Weisman CS, Celentano DD, Teitelbaum MA, Klassen AC. Cancer screening services for the elderly. Public Health Rep 1989;104:209-14.

15. American Cancer Society. Survey of physicians’ attitudes and practices in early cancer detection. Cancer 1990;40:77-101.

16. Roetzheim RG, Pal N, Gonzalez EC, et al. The effects of physician supply on the early detection of colorectal cancer. J Fam Pract 1999;48:850-88.

17. Laish-Vaturi A, Gutman H. Cancer of the anus. Oncol Rep 1998;5:1525-29.

18. Kindig DA, Cultice JM, Mullan F. The elusive generalist physician: can we reach a 50% goal? JAMA 1993;270:1069-73.

19. Rivo ML, Satcher D. Improving access to health care through physician workforce reform: directions for the 21st century. JAMA 1993;270:1074-78.

20. Rivo ML, Mays HL, Katzoff J, Kindig DA. Managed health care: implications for the physician workforce and medical education. Council on Graduate Medical Education. JAMA 1995;274:712-15.

21. Rosenblatt RA. Specialists or generalists: on whom should we base the American health care system? JAMA 1992;267:1665-66.

22. Schroeder SA, Sandy LG. Specialty distribution of U.S. physicians—the invisible driver of health care costs. N Engl J Med 1993;328:961-63.

23. Weiner JP. Forecasting the effects of health reform on US physician workforce requirement: evidence from HMO staffing patterns. JAMA 1994;272:222-30.

24. Barnett PG, Midtling JE. Public policy and the supply of primary care physicians. JAMA 1989;262:2864-68.

25. Barondess JA. Specialization and the physician workforce: drivers and determinants. JAMA 2000;284:1299-301.

26. Kane R, Friedman B. State variations in medicare expenditures. Am J Public Health 1997;87:1611-20.

27. Mark DH, Gottlieb MS, Zellner BB, Chetty VK, Midtling JE. Medicare costs in urban areas and the supply of primary care physicians. J Fam Pract 1996;43:33-39.

28. Welch WP, Miller ME, Welch HG, Fisher ES, Wennberg JE. Geographic variation in expenditures for physicians’ services in the united states. N Engl J Med 1993;328:621-27.

29. Parchman ML, Culler S. Primary care physicians and avoidable hospitalizations. J Fam Pract 1994;39:123-28.

30. Krakauer H, Jacoby I, Millman M, Lukomnik JE. Physician impact on hospital admission and on mortality rates in the Medicare population. Health Serv Res 1996;31:191-211.

31. Krishan I, Drummond DC, Naessens JM, Nobrega FT, Smoldt RK. Impact of increased physician supply on use of health services: a longitudinal analysis in rural Minnesota. Public Health Rep 1985;100:379-86.

32. Briggs LW, Rohrer JE, Ludke RL, Hilsenrath PE, Phillips KT. Geographic variation in primary care visits in Iowa. Health Serv Res 1995;30:657-71.

33. Williams AP, Schwartz WB, Newhouse JP, Bennett BW. How many miles to the doctor? N Engl J Med 1983;309:958-63.

34. Allen DI, Kamradt JM. Relationship of infant mortality to the availability of obstetrical care in Indiana. J Fam Pract 1991;33:609-13.

35. Roetzheim RG, Pal N, Van Durme DJ, et al. Increasing supplies of dermatologists and family physicians are associated with earlier stage of melanoma detection. J Am Acad Derm 2000;43:211-18.

36. Ferrante JM, Gonzalez EC, Pal N, Roetzheim RG. The effects of physician supply on the early detection of breast cancer. J Am Board Fam Pract 2000;13:408-14.

37. Samet JM, Hunt WC, Goodwin JS. Determinants of cancer stage: a population-based study of elderly New Mexicans. Cancer 1990;66:1302-07.

38. Greene J. Emerging specialist shortage triggers workforce review. Am Med News 2001;13-14.

Author and Disclosure Information

Richard G. Roetzheim, MD, MSPH
Eduardo C. Gonzalez, MD
Arnold Ramirez, MD
Robert Campbell, MD
Daniel J. Van Durme, MD
Tampa, Florida
Submitted, revised, May 10, 2001.
From the Department of Family Medicine and the H. Lee Moffitt Cancer Center and Research Institute (R.G.R.) and the Department of Family Medicine (E.C.G., A.R., R.C., D.J.vD.), University of South Florida. Reprint requests should be addressed to Richard Roetzheim, MD, MSPH, University of South Florida, Department of Family Medicine, 12901 Bruce B. Downs Blvd, MDC 13, Tampa, FL 33612. E-mail: rroetzhe@hsc.usf.edu.

Issue
The Journal of Family Practice - 50(12)
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1027-1031
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,Colorectal neoplasmsphysicians, familyhealth manpowerhealth services accessibility. (J Fam Pract 2001; 50:1027-1031)
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Author and Disclosure Information

Richard G. Roetzheim, MD, MSPH
Eduardo C. Gonzalez, MD
Arnold Ramirez, MD
Robert Campbell, MD
Daniel J. Van Durme, MD
Tampa, Florida
Submitted, revised, May 10, 2001.
From the Department of Family Medicine and the H. Lee Moffitt Cancer Center and Research Institute (R.G.R.) and the Department of Family Medicine (E.C.G., A.R., R.C., D.J.vD.), University of South Florida. Reprint requests should be addressed to Richard Roetzheim, MD, MSPH, University of South Florida, Department of Family Medicine, 12901 Bruce B. Downs Blvd, MDC 13, Tampa, FL 33612. E-mail: rroetzhe@hsc.usf.edu.

Author and Disclosure Information

Richard G. Roetzheim, MD, MSPH
Eduardo C. Gonzalez, MD
Arnold Ramirez, MD
Robert Campbell, MD
Daniel J. Van Durme, MD
Tampa, Florida
Submitted, revised, May 10, 2001.
From the Department of Family Medicine and the H. Lee Moffitt Cancer Center and Research Institute (R.G.R.) and the Department of Family Medicine (E.C.G., A.R., R.C., D.J.vD.), University of South Florida. Reprint requests should be addressed to Richard Roetzheim, MD, MSPH, University of South Florida, Department of Family Medicine, 12901 Bruce B. Downs Blvd, MDC 13, Tampa, FL 33612. E-mail: rroetzhe@hsc.usf.edu.

OBJECTIVE: Our goal was to determine if increasing primary care physician supply was associated with lower incidence and mortality rates for colorectal cancer.

STUDY DESIGN: We performed an ecologic study of Florida’s 67 counties, using data from the state tumor registry and the American Medical Association physician masterfile.

POPULATION: Florida residents were included.

OUTCOMES MEASURED: We measured age-adjusted colorectal cancer incidence and mortality rates for Florida’s 67 counties during the period 1993 to 1995.

RESULTS: Increasing primary care physician supply was negatively correlated with both colorectal cancer (CC) incidence (CC = -0.46; P < .001) and mortality rates (CC = -0.29; P =.02). In linear regression that controlled for other county characteristics, each 1% increase in the proportion of county physicians who were in primary care specialties was associated with a corresponding reduction in colorectal cancer incidence of 0.25 cases per 100,000 (P < .001) and a reduction in colorectal cancer mortality of 0.08 cases per 100,000 (P=.008).

CONCLUSIONS: Incidence and mortality of colorectal cancer decreased in Florida counties that had an increased supply of primary care physicians. This suggests that a balanced work force may achieve better health outcomes.

It was predicted that more than 130,000 Americans would develop colorectal cancer in the year 2000. This is the second leading cause of cancer mortality in the United States, with an estimated 56,300 deaths predicted for 2000.1 In that year, the state of Florida ranked third in the number of colorectal cancer cases (9100) and colorectal cancer deaths (3900).

Earlier diagnosis of colorectal cancer, with subsequently reduced mortality, can be achieved by eliciting and promptly evaluating signs and symptoms of colorectal cancer and by providing recommended screening tests, such as fecal occult blood testing and flexible sigmoidoscopy.2 Also, the provision of screening tests may reduce colorectal cancer incidence by detecting and eliminating precancerous polyps. Annual fecal occult blood testing, for example, has been demonstrated to reduce colorectal cancer incidence by 20%.3 Polyps found by screening sigmoidoscopy would also generally result in surveillance colonoscopy, a procedure which may reduce colorectal cancer incidence by as much as 90%.4

Studies have consistently reported that access to health care and a physician’s recommendation for screening are important predictors of cancer screening.5-10 One would expect, therefore, that the provision of colorectal cancer screening tests would be dependent to some extent on the availability of physician services. Physician specialties may differ, however, in their provision of preventive health services. Stange and colleagues,11 for example, found that family physicians addressed at least one US Preventive Services Task Force recommendation for preventive care in 39% of visits for chronic illness. In contrast, evidence suggests that most specialists are not likely to address health care needs outside their specialty.12

Compared with other cancer screening tests, colorectal cancer screening is less frequently recommended by physicians and is less frequently completed by patients. It is possible, therefore, that the availability of primary care providers has relatively limited impact on colorectal cancer outcomes.13-15 We have previously shown that increasing supplies of primary care physicians were associated with earlier detection of colorectal cancer, while increasing supplies of non–primary care physicians were associated with later-stage diagnosis.16 We hypothesized, therefore, that increasing primary care physician supply would also be associated with lower incidence and mortality rates for colorectal cancer.

Methods

We performed an ecologic study comparing primary care physician supply with colorectal cancer incidence and mortality rates. Colorectal cancer incidence and mortality rates for Florida’s 67 counties were identified using the Florida Cancer Data System (FCDS), a population-based statewide cancer registry. The FCDS is a member of the North American Association of Central Cancer Registries (NAACCR). NAACCR audits have estimated that the completeness of case ascertainment for the period 1990 to 1994 is 99.7%. The FCDS provides age-adjusted incidence and mortality rates by standardizing them to the 1970 US standard population. To account for year-to-year fluctuations, rates were averaged over the 3-year period 1993 to 1995.

Because distal cancers may be more easily detected with screening tests such as sigmoidoscopy, we also examined incidence rates stratified by proximal versus distal origin of the cancer. We defined proximal cancers as those arising from the cecum, ascending colon, hepatic flexure, transverse colon, and splenic flexure. Distal cancers were defined as those arising from the descending colon, sigmoid colon, rectosigmoid juncture, and the rectum. Tumors of the anal canal were excluded because of differing pathology and treatment implications.17

We used the 1990 US census to ascertain other characteristics of Florida counties that might have an impact on colorectal cancer incidence and mortality. In addition to age, colorectal cancer incidence and mortality rates vary by race, socioeconomic status, and marital status. Variables obtained for each county included median household income, percentage of county residents with less than a high school education, percentage residing in urban census areas, percentage who were white, and percentage who were married.

 

 

Data on physician supply were obtained from the 1994 American Medical Association (AMA) physician masterfile, which includes allopathic and osteopathic physicians regardless of AMA membership. County-level population estimates were obtained from the 1990 United States Census. Physician supply variables were created for total physician supply, and for primary care physician supply and non–primary care physician supply. Physicians were classified as primary care if their self-designated specialty was family practice, general practice, obstetrics/gynecology, or general internal medicine.

Physicians who indicated they were engaged in full-time direct patient care were counted as one full-time equivalent (FTE); those who indicated in the masterfile that they were either “semi-retired,” in residency training, or engaged in teaching or research were counted as 0.5 FTE. Physicians who indicated they were no longer involved in direct patient care were excluded. On the basis of this information, we calculated for each county the proportion of all physicians engaged in primary care and used this as our measure of primary care supply.

Counties were the unit of analysis for our study. We explored associations between primary care physician supply, and colorectal cancer incidence and mortality rates in 2 ways. First we constructed scatterplots to explore possible linear relationships, and to exclude nonlinear associations, and also calculated Pearson correlation coefficients. Second, we used multiple linear regression to explore the multivariable relationship between primary care physician supply and outcomes, controlling for other county-level characteristics.

Parameter estimates were determined using the method of ordinary least squares. Potential confounding variables included in each initial model were median household income, percentage of county residents with less than a high school education, percentage residing in urban census areas, percentage who were white, percentage who were married, and total physician supply. Final regression models included all variables that remained statistically significant (P < .05), using a backward variable selection algorithm. We also confirmed that all outcomes were normally distributed using graphical methods.

Results

The average physician supply for Florida’s 67 counties (physicians per 100,000 population) was 134.9, with primary care supply at 49.7 and specialist supply at 85.2. The average supply of primary care specialties was as follows: family physicians, 17.5; general practitioners, 10.7; general internists, 13.9; and obstetrician-gynecologists, 7.2. There was substantial variation in physician supply, with some counties having as few as 15 physicians per 100,000 population and other counties having more than 500 physicians per 100,000 population. The average proportion of physicians who were in a primary care specialty was 0.36 across Florida’s 67 counties (standard deviation = 0.19; range = 0.17-1.00).

There was also substantial variation in both incidence and mortality rates across Florida’s 67 counties. Some counties had incidence rates as low as 9.6 cases per 100,000 and others as high as 72 cases per 100,000. Mortality rates varied from a low of 3.8 cases per 100,000 to a high of 26.4 cases per 100,000. Incidence and mortality rates were both higher in men than in women.

Associations between primary care physician supply and colorectal cancer incidence and mortality rates were assessed both graphically and using the Pearson correlation coefficient Table 1.* ( Figure 1, Figure 2, Figure 3) Primary care physician supply was negatively correlated with colorectal cancer incidence and mortality rates in the 67 counties studied. For colorectal cancer incidence rates, negative correlations were observed for both proximal and distal cancers, and among both men and women. For mortality rates, correlations were stronger for men and did not reach statistical significance among women. Scatter diagrams did not suggest the presence of nonlinear relationships.

Table 2 presents the results of linear regression analyses. Primary care physician supply was a statistically significant predictor of all outcomes examined. Each 1% increase in primary care physician supply was associated with a reduction in overall colorectal cancer incidence of 0.25 cases per 100,000. Each 1% increase in primary care physician supply was similarly associated with a reduction in overall colorectal cancer mortality of 0.08 cases per 100,000. In stratified analysis, primary care physician supply had similar effects for both proximal and distal cancers, with slightly greater effects among men than women. Overall physician supply was not a significant predictor of any of the outcomes examined.

Discussion

We found that an increasing supply of primary care physicians was associated with lower incidence and lower mortality rates of colorectal cancer in Florida counties. Each 1% increase in primary care physician supply was associated with a reduction in colorectal cancer incidence of 0.25 cases per 100,000 and a reduction in mortality of 0.08 cases per 100,000. In contrast, overall physician supply was unrelated to any of the outcomes examined. Findings were similar in men and women and for proximal and distal cancers.

 

 

Although there is continued interest in the composition of the United States physician work force,18-25 there have been surprisingly few studies demonstrating the effects of physician supply on health-related outcomes. Some studies have suggested that an oversupply of specialists may contribute to higher health care costs.22,26-28 Primary care physician supply has been correlated with reduced hospitalization rates for ambulatory care–sensitive conditions29,30 and with improved access and overall use of ambulatory health services.31-34

We have previously shown associations between primary care physician supply and earlier detection of breast cancer, colorectal cancer, and malignant melanoma.16,35,36 These findings are consistent with studies showing that patients who have a family physician are more likely to receive a diagnosis of early-stage cancer.37 Our study suggests that increasing supplies of primary care physicians might also be associated with reduced incidence and mortality for some cancers. In contrast, increased overall supplies of physicians have not been associated with improved cancer outcomes, suggesting that a balanced physician work force may be necessary to achieve optimal health outcomes.

Physician specialty choice and practice location are driven by many factors, including the location of training programs at medical schools and residencies, role models in medical school, education debt, lifestyle, and other issues. These factors influence the types of physicians that practice in various locations, and as a result may influence the health care of the population in that area. As the physician work force is studied and policy decisions are made, it will be important to consider measurable health care outcomes in addition to projected demands based on economic forces.38

Limitations

This study has a number of important limitations that should be considered. First, ecologic studies are subject to the ecologic fallacy, in which associations at the population level do not accurately reflect associations at the individual level. We did not have information on individual patients’ actual use of physician services, for example, so patients’ actual access to primary care may have been different than that predicted by county-level measures. Ecologic studies have very limited ability to establish causation, and follow-up studies conducted at the individual patient level (such as case-control or cohort studies) will be necessary to confirm these findings. The exploratory nature of selecting variables for ecologic studies may also increase type 1 statistical errors, falsely concluding that associations exist when they have actually occurred by chance.

We did not have information on other colorectal cancer risk factors, such as dietary patterns, rates of family history, or rates of ulcerative colitis. We also lacked information on rates of detection of precancerous polyps, and the age/sex distribution of physicians, which would have strengthened our study. Because incidence and mortality rates were established according to the patient’s county of residence rather than the location of diagnosis or treatment, we do not believe the associations observed were the result of referral patterns (eg, patients with suspected late-stage disease being referred to areas with higher-specialty physician supply). However, physician supply might be correlated with other unmeasured characteristics of our health care delivery system, which could account for the observed associations. Finally, our study was restricted to colorectal cancer in Florida, which may not be representative of other diseases or other parts of the country.

Conclusions

Both the incidence and mortality of colorectal cancer were decreased in Florida counties that had a greater supply of primary care physicians. Overall physician supply, however, was unrelated to colorectal cancer mortality or incidence. These associations will need to be confirmed with studies conducted at the individual level.

OBJECTIVE: Our goal was to determine if increasing primary care physician supply was associated with lower incidence and mortality rates for colorectal cancer.

STUDY DESIGN: We performed an ecologic study of Florida’s 67 counties, using data from the state tumor registry and the American Medical Association physician masterfile.

POPULATION: Florida residents were included.

OUTCOMES MEASURED: We measured age-adjusted colorectal cancer incidence and mortality rates for Florida’s 67 counties during the period 1993 to 1995.

RESULTS: Increasing primary care physician supply was negatively correlated with both colorectal cancer (CC) incidence (CC = -0.46; P < .001) and mortality rates (CC = -0.29; P =.02). In linear regression that controlled for other county characteristics, each 1% increase in the proportion of county physicians who were in primary care specialties was associated with a corresponding reduction in colorectal cancer incidence of 0.25 cases per 100,000 (P < .001) and a reduction in colorectal cancer mortality of 0.08 cases per 100,000 (P=.008).

CONCLUSIONS: Incidence and mortality of colorectal cancer decreased in Florida counties that had an increased supply of primary care physicians. This suggests that a balanced work force may achieve better health outcomes.

It was predicted that more than 130,000 Americans would develop colorectal cancer in the year 2000. This is the second leading cause of cancer mortality in the United States, with an estimated 56,300 deaths predicted for 2000.1 In that year, the state of Florida ranked third in the number of colorectal cancer cases (9100) and colorectal cancer deaths (3900).

Earlier diagnosis of colorectal cancer, with subsequently reduced mortality, can be achieved by eliciting and promptly evaluating signs and symptoms of colorectal cancer and by providing recommended screening tests, such as fecal occult blood testing and flexible sigmoidoscopy.2 Also, the provision of screening tests may reduce colorectal cancer incidence by detecting and eliminating precancerous polyps. Annual fecal occult blood testing, for example, has been demonstrated to reduce colorectal cancer incidence by 20%.3 Polyps found by screening sigmoidoscopy would also generally result in surveillance colonoscopy, a procedure which may reduce colorectal cancer incidence by as much as 90%.4

Studies have consistently reported that access to health care and a physician’s recommendation for screening are important predictors of cancer screening.5-10 One would expect, therefore, that the provision of colorectal cancer screening tests would be dependent to some extent on the availability of physician services. Physician specialties may differ, however, in their provision of preventive health services. Stange and colleagues,11 for example, found that family physicians addressed at least one US Preventive Services Task Force recommendation for preventive care in 39% of visits for chronic illness. In contrast, evidence suggests that most specialists are not likely to address health care needs outside their specialty.12

Compared with other cancer screening tests, colorectal cancer screening is less frequently recommended by physicians and is less frequently completed by patients. It is possible, therefore, that the availability of primary care providers has relatively limited impact on colorectal cancer outcomes.13-15 We have previously shown that increasing supplies of primary care physicians were associated with earlier detection of colorectal cancer, while increasing supplies of non–primary care physicians were associated with later-stage diagnosis.16 We hypothesized, therefore, that increasing primary care physician supply would also be associated with lower incidence and mortality rates for colorectal cancer.

Methods

We performed an ecologic study comparing primary care physician supply with colorectal cancer incidence and mortality rates. Colorectal cancer incidence and mortality rates for Florida’s 67 counties were identified using the Florida Cancer Data System (FCDS), a population-based statewide cancer registry. The FCDS is a member of the North American Association of Central Cancer Registries (NAACCR). NAACCR audits have estimated that the completeness of case ascertainment for the period 1990 to 1994 is 99.7%. The FCDS provides age-adjusted incidence and mortality rates by standardizing them to the 1970 US standard population. To account for year-to-year fluctuations, rates were averaged over the 3-year period 1993 to 1995.

Because distal cancers may be more easily detected with screening tests such as sigmoidoscopy, we also examined incidence rates stratified by proximal versus distal origin of the cancer. We defined proximal cancers as those arising from the cecum, ascending colon, hepatic flexure, transverse colon, and splenic flexure. Distal cancers were defined as those arising from the descending colon, sigmoid colon, rectosigmoid juncture, and the rectum. Tumors of the anal canal were excluded because of differing pathology and treatment implications.17

We used the 1990 US census to ascertain other characteristics of Florida counties that might have an impact on colorectal cancer incidence and mortality. In addition to age, colorectal cancer incidence and mortality rates vary by race, socioeconomic status, and marital status. Variables obtained for each county included median household income, percentage of county residents with less than a high school education, percentage residing in urban census areas, percentage who were white, and percentage who were married.

 

 

Data on physician supply were obtained from the 1994 American Medical Association (AMA) physician masterfile, which includes allopathic and osteopathic physicians regardless of AMA membership. County-level population estimates were obtained from the 1990 United States Census. Physician supply variables were created for total physician supply, and for primary care physician supply and non–primary care physician supply. Physicians were classified as primary care if their self-designated specialty was family practice, general practice, obstetrics/gynecology, or general internal medicine.

Physicians who indicated they were engaged in full-time direct patient care were counted as one full-time equivalent (FTE); those who indicated in the masterfile that they were either “semi-retired,” in residency training, or engaged in teaching or research were counted as 0.5 FTE. Physicians who indicated they were no longer involved in direct patient care were excluded. On the basis of this information, we calculated for each county the proportion of all physicians engaged in primary care and used this as our measure of primary care supply.

Counties were the unit of analysis for our study. We explored associations between primary care physician supply, and colorectal cancer incidence and mortality rates in 2 ways. First we constructed scatterplots to explore possible linear relationships, and to exclude nonlinear associations, and also calculated Pearson correlation coefficients. Second, we used multiple linear regression to explore the multivariable relationship between primary care physician supply and outcomes, controlling for other county-level characteristics.

Parameter estimates were determined using the method of ordinary least squares. Potential confounding variables included in each initial model were median household income, percentage of county residents with less than a high school education, percentage residing in urban census areas, percentage who were white, percentage who were married, and total physician supply. Final regression models included all variables that remained statistically significant (P < .05), using a backward variable selection algorithm. We also confirmed that all outcomes were normally distributed using graphical methods.

Results

The average physician supply for Florida’s 67 counties (physicians per 100,000 population) was 134.9, with primary care supply at 49.7 and specialist supply at 85.2. The average supply of primary care specialties was as follows: family physicians, 17.5; general practitioners, 10.7; general internists, 13.9; and obstetrician-gynecologists, 7.2. There was substantial variation in physician supply, with some counties having as few as 15 physicians per 100,000 population and other counties having more than 500 physicians per 100,000 population. The average proportion of physicians who were in a primary care specialty was 0.36 across Florida’s 67 counties (standard deviation = 0.19; range = 0.17-1.00).

There was also substantial variation in both incidence and mortality rates across Florida’s 67 counties. Some counties had incidence rates as low as 9.6 cases per 100,000 and others as high as 72 cases per 100,000. Mortality rates varied from a low of 3.8 cases per 100,000 to a high of 26.4 cases per 100,000. Incidence and mortality rates were both higher in men than in women.

Associations between primary care physician supply and colorectal cancer incidence and mortality rates were assessed both graphically and using the Pearson correlation coefficient Table 1.* ( Figure 1, Figure 2, Figure 3) Primary care physician supply was negatively correlated with colorectal cancer incidence and mortality rates in the 67 counties studied. For colorectal cancer incidence rates, negative correlations were observed for both proximal and distal cancers, and among both men and women. For mortality rates, correlations were stronger for men and did not reach statistical significance among women. Scatter diagrams did not suggest the presence of nonlinear relationships.

Table 2 presents the results of linear regression analyses. Primary care physician supply was a statistically significant predictor of all outcomes examined. Each 1% increase in primary care physician supply was associated with a reduction in overall colorectal cancer incidence of 0.25 cases per 100,000. Each 1% increase in primary care physician supply was similarly associated with a reduction in overall colorectal cancer mortality of 0.08 cases per 100,000. In stratified analysis, primary care physician supply had similar effects for both proximal and distal cancers, with slightly greater effects among men than women. Overall physician supply was not a significant predictor of any of the outcomes examined.

Discussion

We found that an increasing supply of primary care physicians was associated with lower incidence and lower mortality rates of colorectal cancer in Florida counties. Each 1% increase in primary care physician supply was associated with a reduction in colorectal cancer incidence of 0.25 cases per 100,000 and a reduction in mortality of 0.08 cases per 100,000. In contrast, overall physician supply was unrelated to any of the outcomes examined. Findings were similar in men and women and for proximal and distal cancers.

 

 

Although there is continued interest in the composition of the United States physician work force,18-25 there have been surprisingly few studies demonstrating the effects of physician supply on health-related outcomes. Some studies have suggested that an oversupply of specialists may contribute to higher health care costs.22,26-28 Primary care physician supply has been correlated with reduced hospitalization rates for ambulatory care–sensitive conditions29,30 and with improved access and overall use of ambulatory health services.31-34

We have previously shown associations between primary care physician supply and earlier detection of breast cancer, colorectal cancer, and malignant melanoma.16,35,36 These findings are consistent with studies showing that patients who have a family physician are more likely to receive a diagnosis of early-stage cancer.37 Our study suggests that increasing supplies of primary care physicians might also be associated with reduced incidence and mortality for some cancers. In contrast, increased overall supplies of physicians have not been associated with improved cancer outcomes, suggesting that a balanced physician work force may be necessary to achieve optimal health outcomes.

Physician specialty choice and practice location are driven by many factors, including the location of training programs at medical schools and residencies, role models in medical school, education debt, lifestyle, and other issues. These factors influence the types of physicians that practice in various locations, and as a result may influence the health care of the population in that area. As the physician work force is studied and policy decisions are made, it will be important to consider measurable health care outcomes in addition to projected demands based on economic forces.38

Limitations

This study has a number of important limitations that should be considered. First, ecologic studies are subject to the ecologic fallacy, in which associations at the population level do not accurately reflect associations at the individual level. We did not have information on individual patients’ actual use of physician services, for example, so patients’ actual access to primary care may have been different than that predicted by county-level measures. Ecologic studies have very limited ability to establish causation, and follow-up studies conducted at the individual patient level (such as case-control or cohort studies) will be necessary to confirm these findings. The exploratory nature of selecting variables for ecologic studies may also increase type 1 statistical errors, falsely concluding that associations exist when they have actually occurred by chance.

We did not have information on other colorectal cancer risk factors, such as dietary patterns, rates of family history, or rates of ulcerative colitis. We also lacked information on rates of detection of precancerous polyps, and the age/sex distribution of physicians, which would have strengthened our study. Because incidence and mortality rates were established according to the patient’s county of residence rather than the location of diagnosis or treatment, we do not believe the associations observed were the result of referral patterns (eg, patients with suspected late-stage disease being referred to areas with higher-specialty physician supply). However, physician supply might be correlated with other unmeasured characteristics of our health care delivery system, which could account for the observed associations. Finally, our study was restricted to colorectal cancer in Florida, which may not be representative of other diseases or other parts of the country.

Conclusions

Both the incidence and mortality of colorectal cancer were decreased in Florida counties that had a greater supply of primary care physicians. Overall physician supply, however, was unrelated to colorectal cancer mortality or incidence. These associations will need to be confirmed with studies conducted at the individual level.

References

1. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000;50:7-33.

2. United States Preventive Service Task Force. Guide to clinical preventive services. 2nd ed. Washington, DC: US Department of Health and Human Services; 1996.

3. Mandel JS, Church TR, Bond JH, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med 2000;343:1603-07.

4. Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal cancer by colonoscopic polypectomy: The National Polyp Study Workgroup. N Engl J Med 1993;329:1977-81.

5. Fox SA, Murata PJ, Stein JA. The impact of physician compliance on screening mammography for older women. Arch Intern Med 1991;151:50-56.

6. Fox SA, Siu AL, Stein JA. The importance of physician communication on breast cancer screening of older women. Arch Intern Med 1994;154:2058-68.

7. Breen N, Kessler L. Changes in the use of screening mammography: evidence from the 1987 and 1990 National Health Interview Surveys. Am J Public Health 1994;84:62-67.

8. National Cancer Institute Breast Cancer Screening Consortium. Screening mammography: a missed clinical opportunity? JAMA 1990;264:54-58.

9. Lewis SF, Jensen NM. Screening sigmoidoscopy: factors associated with utilization. J Gen Intern Med 1996;11:542-44.

10. Vernon S. Participation in colorectal cancer screening: a review. J Natl Cancer Inst 1997;89:1406-22.

11. Stange K, Flocke S, Goodwin M. Opportunistic preventive services delivery. J Fam Pract 1998;46:419-24.

12. Rosenblatt RA, Hart LG, Baldwin LM, Chan L, Schneeweiss R. The generalist role of specialty physicians: is there a hidden system of primary care? JAMA 1998;279:1364-70.

13. Brownson RC, Davis JR, Simms SG, Kern TG, Harmon RG. Cancer control knowledge and priorities among primary care physicians. J Cancer Educ 1993;8:35-41.

14. Weisman CS, Celentano DD, Teitelbaum MA, Klassen AC. Cancer screening services for the elderly. Public Health Rep 1989;104:209-14.

15. American Cancer Society. Survey of physicians’ attitudes and practices in early cancer detection. Cancer 1990;40:77-101.

16. Roetzheim RG, Pal N, Gonzalez EC, et al. The effects of physician supply on the early detection of colorectal cancer. J Fam Pract 1999;48:850-88.

17. Laish-Vaturi A, Gutman H. Cancer of the anus. Oncol Rep 1998;5:1525-29.

18. Kindig DA, Cultice JM, Mullan F. The elusive generalist physician: can we reach a 50% goal? JAMA 1993;270:1069-73.

19. Rivo ML, Satcher D. Improving access to health care through physician workforce reform: directions for the 21st century. JAMA 1993;270:1074-78.

20. Rivo ML, Mays HL, Katzoff J, Kindig DA. Managed health care: implications for the physician workforce and medical education. Council on Graduate Medical Education. JAMA 1995;274:712-15.

21. Rosenblatt RA. Specialists or generalists: on whom should we base the American health care system? JAMA 1992;267:1665-66.

22. Schroeder SA, Sandy LG. Specialty distribution of U.S. physicians—the invisible driver of health care costs. N Engl J Med 1993;328:961-63.

23. Weiner JP. Forecasting the effects of health reform on US physician workforce requirement: evidence from HMO staffing patterns. JAMA 1994;272:222-30.

24. Barnett PG, Midtling JE. Public policy and the supply of primary care physicians. JAMA 1989;262:2864-68.

25. Barondess JA. Specialization and the physician workforce: drivers and determinants. JAMA 2000;284:1299-301.

26. Kane R, Friedman B. State variations in medicare expenditures. Am J Public Health 1997;87:1611-20.

27. Mark DH, Gottlieb MS, Zellner BB, Chetty VK, Midtling JE. Medicare costs in urban areas and the supply of primary care physicians. J Fam Pract 1996;43:33-39.

28. Welch WP, Miller ME, Welch HG, Fisher ES, Wennberg JE. Geographic variation in expenditures for physicians’ services in the united states. N Engl J Med 1993;328:621-27.

29. Parchman ML, Culler S. Primary care physicians and avoidable hospitalizations. J Fam Pract 1994;39:123-28.

30. Krakauer H, Jacoby I, Millman M, Lukomnik JE. Physician impact on hospital admission and on mortality rates in the Medicare population. Health Serv Res 1996;31:191-211.

31. Krishan I, Drummond DC, Naessens JM, Nobrega FT, Smoldt RK. Impact of increased physician supply on use of health services: a longitudinal analysis in rural Minnesota. Public Health Rep 1985;100:379-86.

32. Briggs LW, Rohrer JE, Ludke RL, Hilsenrath PE, Phillips KT. Geographic variation in primary care visits in Iowa. Health Serv Res 1995;30:657-71.

33. Williams AP, Schwartz WB, Newhouse JP, Bennett BW. How many miles to the doctor? N Engl J Med 1983;309:958-63.

34. Allen DI, Kamradt JM. Relationship of infant mortality to the availability of obstetrical care in Indiana. J Fam Pract 1991;33:609-13.

35. Roetzheim RG, Pal N, Van Durme DJ, et al. Increasing supplies of dermatologists and family physicians are associated with earlier stage of melanoma detection. J Am Acad Derm 2000;43:211-18.

36. Ferrante JM, Gonzalez EC, Pal N, Roetzheim RG. The effects of physician supply on the early detection of breast cancer. J Am Board Fam Pract 2000;13:408-14.

37. Samet JM, Hunt WC, Goodwin JS. Determinants of cancer stage: a population-based study of elderly New Mexicans. Cancer 1990;66:1302-07.

38. Greene J. Emerging specialist shortage triggers workforce review. Am Med News 2001;13-14.

References

1. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000;50:7-33.

2. United States Preventive Service Task Force. Guide to clinical preventive services. 2nd ed. Washington, DC: US Department of Health and Human Services; 1996.

3. Mandel JS, Church TR, Bond JH, et al. The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med 2000;343:1603-07.

4. Winawer SJ, Zauber AG, Ho MN, et al. Prevention of colorectal cancer by colonoscopic polypectomy: The National Polyp Study Workgroup. N Engl J Med 1993;329:1977-81.

5. Fox SA, Murata PJ, Stein JA. The impact of physician compliance on screening mammography for older women. Arch Intern Med 1991;151:50-56.

6. Fox SA, Siu AL, Stein JA. The importance of physician communication on breast cancer screening of older women. Arch Intern Med 1994;154:2058-68.

7. Breen N, Kessler L. Changes in the use of screening mammography: evidence from the 1987 and 1990 National Health Interview Surveys. Am J Public Health 1994;84:62-67.

8. National Cancer Institute Breast Cancer Screening Consortium. Screening mammography: a missed clinical opportunity? JAMA 1990;264:54-58.

9. Lewis SF, Jensen NM. Screening sigmoidoscopy: factors associated with utilization. J Gen Intern Med 1996;11:542-44.

10. Vernon S. Participation in colorectal cancer screening: a review. J Natl Cancer Inst 1997;89:1406-22.

11. Stange K, Flocke S, Goodwin M. Opportunistic preventive services delivery. J Fam Pract 1998;46:419-24.

12. Rosenblatt RA, Hart LG, Baldwin LM, Chan L, Schneeweiss R. The generalist role of specialty physicians: is there a hidden system of primary care? JAMA 1998;279:1364-70.

13. Brownson RC, Davis JR, Simms SG, Kern TG, Harmon RG. Cancer control knowledge and priorities among primary care physicians. J Cancer Educ 1993;8:35-41.

14. Weisman CS, Celentano DD, Teitelbaum MA, Klassen AC. Cancer screening services for the elderly. Public Health Rep 1989;104:209-14.

15. American Cancer Society. Survey of physicians’ attitudes and practices in early cancer detection. Cancer 1990;40:77-101.

16. Roetzheim RG, Pal N, Gonzalez EC, et al. The effects of physician supply on the early detection of colorectal cancer. J Fam Pract 1999;48:850-88.

17. Laish-Vaturi A, Gutman H. Cancer of the anus. Oncol Rep 1998;5:1525-29.

18. Kindig DA, Cultice JM, Mullan F. The elusive generalist physician: can we reach a 50% goal? JAMA 1993;270:1069-73.

19. Rivo ML, Satcher D. Improving access to health care through physician workforce reform: directions for the 21st century. JAMA 1993;270:1074-78.

20. Rivo ML, Mays HL, Katzoff J, Kindig DA. Managed health care: implications for the physician workforce and medical education. Council on Graduate Medical Education. JAMA 1995;274:712-15.

21. Rosenblatt RA. Specialists or generalists: on whom should we base the American health care system? JAMA 1992;267:1665-66.

22. Schroeder SA, Sandy LG. Specialty distribution of U.S. physicians—the invisible driver of health care costs. N Engl J Med 1993;328:961-63.

23. Weiner JP. Forecasting the effects of health reform on US physician workforce requirement: evidence from HMO staffing patterns. JAMA 1994;272:222-30.

24. Barnett PG, Midtling JE. Public policy and the supply of primary care physicians. JAMA 1989;262:2864-68.

25. Barondess JA. Specialization and the physician workforce: drivers and determinants. JAMA 2000;284:1299-301.

26. Kane R, Friedman B. State variations in medicare expenditures. Am J Public Health 1997;87:1611-20.

27. Mark DH, Gottlieb MS, Zellner BB, Chetty VK, Midtling JE. Medicare costs in urban areas and the supply of primary care physicians. J Fam Pract 1996;43:33-39.

28. Welch WP, Miller ME, Welch HG, Fisher ES, Wennberg JE. Geographic variation in expenditures for physicians’ services in the united states. N Engl J Med 1993;328:621-27.

29. Parchman ML, Culler S. Primary care physicians and avoidable hospitalizations. J Fam Pract 1994;39:123-28.

30. Krakauer H, Jacoby I, Millman M, Lukomnik JE. Physician impact on hospital admission and on mortality rates in the Medicare population. Health Serv Res 1996;31:191-211.

31. Krishan I, Drummond DC, Naessens JM, Nobrega FT, Smoldt RK. Impact of increased physician supply on use of health services: a longitudinal analysis in rural Minnesota. Public Health Rep 1985;100:379-86.

32. Briggs LW, Rohrer JE, Ludke RL, Hilsenrath PE, Phillips KT. Geographic variation in primary care visits in Iowa. Health Serv Res 1995;30:657-71.

33. Williams AP, Schwartz WB, Newhouse JP, Bennett BW. How many miles to the doctor? N Engl J Med 1983;309:958-63.

34. Allen DI, Kamradt JM. Relationship of infant mortality to the availability of obstetrical care in Indiana. J Fam Pract 1991;33:609-13.

35. Roetzheim RG, Pal N, Van Durme DJ, et al. Increasing supplies of dermatologists and family physicians are associated with earlier stage of melanoma detection. J Am Acad Derm 2000;43:211-18.

36. Ferrante JM, Gonzalez EC, Pal N, Roetzheim RG. The effects of physician supply on the early detection of breast cancer. J Am Board Fam Pract 2000;13:408-14.

37. Samet JM, Hunt WC, Goodwin JS. Determinants of cancer stage: a population-based study of elderly New Mexicans. Cancer 1990;66:1302-07.

38. Greene J. Emerging specialist shortage triggers workforce review. Am Med News 2001;13-14.

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