Association between socioeconomic position and diabetic foot ulcer outcomes: a population-based cohort study in South Korea

Diabetic foot ulcers (DFUs) are one of the major complications of neuropathy and microvascular disease in patients with diabetes. The annual incidence and prevalence rates of DFU are 1–4% and 5–10%, respectively, while the lifetime risk of developing DFUs is 15% in diabetic patients [1, 2]. DFUs, the major cause of nontraumatic amputation, are known to have a strong correlation with increased morbidity and mortality [3‐7]. Amputation may lead to social deprivation and great economic cost.

Several medical factors including atherosclerosis with multiple stenosis, nephropathy, and uncontrolled diabetes have been reported as predictive factors for amputation and mortality, which are the major outcomes of DFUs [2, 8]. However, socioeconomic factors may also importantly account for these outcomes because DFUs tend to occur as a result of chronic damage of tissues due to poor diabetes control. Diabetes, like other chronic diseases, is associated with socioeconomic position (SEP) [9‐11]. Although the development of DFUs is associated with a low SEP [12], only a few reports exist on association between SEP and the prognosis of DFUs [13]. Patients with DFUs require additional comprehensive care with collaborations between primary and specialty care as well as more controlled health behavior. Furthermore, the cost associated with DFU treatment is high. A decreasing amputation rate among persons with diabetes has been reported, although a wide gap exists among societies and populations [14‐17].

Equality in health care according to the need has been an important goal for health care policy in South Korea. All citizens of South Korea are covered by a mandatory health insurance system from birth to death. People are designated as National Health Insurance (NHI) or medical aid (MA) beneficiaries according to their insurance status. Most people who are covered under the NHI are associated with a low SEP and are recipients of the National Basic Livelihood Security System in South Korea. Understanding the association between amputation and mortality rate of DFUs with low SEP can lead to the development of health policies that can ameliorate the inequalities among the different SEPs.

This study aimed to determine the association between SEP and DFU outcomes, namely, amputation and mortality, and identify prognostic factors for these outcomes in a South Korean population.

We investigated amputation and mortality rates among patients with DFUs in the South Korean population using the database of the National Health Insurance Sharing Service-National Sample Cohort (NHIS-NSC). The amputation and mortality rates based on residence, type of health insurance, type of medical institution, and income status were examined and the comorbidities associated with diabetes were also considered.

Our study results indicate that a low SEP, reflected by area residence, income level, and type of insurance, is associated with poor outcomes in patients with DFU. Both amputation and mortality rates showed significant differences between the lowest and highest SEP groups. This association was significant after considering age, sex, and comorbidities. Similarly, association between lower SEP and high rate of lower extremity amputation has been reported in peripheral vascular disease [23‐26]. While the pathophysiology of peripheral vascular disease overlaps with DFUs, these studies are in line with our results. According to the institution type at first diagnosis, secondary hospitals showed a significantly higher risk than primary hospitals. This may imply that while the phase of referral to specialists in South Korea was performed without delay, patient-related factors such as SEP may have largely affected the prognosis.

We investigated factors representing biological mediators for amputation including neuropathy and vasculopathy, and disease severity of diabetes including nephropathy ophthalmopathy. Between the biological mediators, the main etiologies of DFU [27], vasculopathy had more significant impact on DFU outcomes. For the variables representing disease severity, ophthalmopathy but not nephropathy significantly predicted the DFU outcomes in multivariable analysis. Although ophthalmopathy and nephropathy are both considered as typical microvascular complication of diabetes, main pathophysiologic mechanism of ophthalmopathy is retinal ischemia associated with abnormal microvasculature while nephropathy has much more complicated pathophysiology besides microcirculation alterations; structural changes of glomerulus, mesangial expansion and tubulointerstitial fibrosis [28]. Also in line with our results, diabetic retinopathy has been reported to be the predictor for other diabetic complications including DFU [29‐33]. These findings consistently suggest that microvascular abnormality in diabetes is the key component in predicting DFU outcomes.

We suggest that poor access to care, processes and quality of care, and health behaviors associated with patient education [9] are potential explanations for our results. Poor access to care may be related to a delayed diagnosis. A low SEP population may not be aware of their foot problem, which impedes their clinical visit. Even though the patient perceives their problem, lack of access to adequate primary and advanced care may result in a delay. Poor processes and quality of care may be related to inappropriate treatment. DFUs require early expert assessment and multidisciplinary management in various aspects including infection, peripheral ischemia, and peripheral neuropathy [6]. Close collaboration and timely referral are essential between primary physicians and specialties to improve outcomes [34]. Physicians without awareness of diabetic foot problems may not closely examine the wound, which delays the referral to specialties. Among patients who were referred to specialties, those with a low SEP had poor accessibility to frequent clinical visits because of cost or location. DFUs account for a large proportion of rising health care costs for persons with diabetes [35, 36]. This would cause difficulty in accessing care for patients with a low SEP. Sporadic clinical visits prevent frequent evaluations, impeding appropriate education and timely management. Delayed diagnosis, inappropriate treatment, and poor compliance worsen DFUs, increasing the risk of amputation and death.

The strength of this study is that its target sample group was randomly selected which can represent the total South Korean population. Although South Korea provides health insurance coverage for all citizens, blind spots exist, especially for diseases that require meticulous care. The findings from investigations into the prevalence of DFUs and the predictive factors for its prognosis, can guide the rational development of appropriate health care policies. According to our study, the low SEP group may be considered a high-risk group for poor DFU outcomes. While DFUs are associated with high health-related costs in persons with diabetes, patients with a low SEP are more likely to be neglected, which makes it a vicious cycle. DFUs, with amputation as the outcome, are associated with higher health-related costs caused by hospitalization, rehabilitation, home care, and social services for the disabled. Therefore, prevention of amputation through appropriate wound care can be the most important step for cost reduction in these patients. Management health programs will be useful for DFU patients with a low SEP, if provided by the society. Many studies have reported that prevention and screening programs for DFUs can reduce the rates of amputation, re-ulceration, and hospitalization [37‐39]. Patout et al. [40] implemented a comprehensive prevention program for lower extremity amputations due to diabetes in Louisiana for low-income African-American populations. This resulted in a profound reduction in DFU-related complications including hospitalization, length of hospital stay, emergency room visits, foot operations, and lower extremity amputations after 1 year. According to a study conducted in the United Kingdom, developing DFU screening and preventive programs cost GB£100,000 (US$160,000) but saved approximately GB£3000 per amputation [41]. In this regard, diabetic foot management programs for DFU patients with a low SEP would largely reduce amputation and mortality rates, which can further reduce health-related costs. Regular foot inspections and education programs can be useful management tools. Education for primary care physicians may also be helpful [42]. The proportion of persons with diabetes undergoing annual foot examination in primary care hospitals is less than 49% [40]. Especially in South Korea, the proportion was even lower than 10% following the reports of 2007 [43]. In another study, of diabetic patients, who were admitted for foot infections, only 14% received fundamental foot examinations [44].

Our study has some limitations. First, our data did not include lifestyle, smoking, or health-related clinical factors such as hemoglobin A1c level and body mass index, which could have influenced the outcomes. Second, although the claims data were available from the year 2002, our study only targeted data from the year 2011 onwards because this was the year when the specific disease code for the diabetic foot was generated. This inevitably reduced the total sample size. Third, major and minor amputation was not separately considered but was analyzed together as amputation event. First amputation event, major or minor, has its value but cannot reflect the severity of the outcome. Forth, death was not investigated in a disease specific manner and further investigation would be required. Lastly, this is a population-based study conducted in South Korea, and its findings may not necessarily be generalizable to the people of other countries with different medical insurance systems. Future studies that consider a more comprehensive range of factors including medication, laboratory data, and lifestyles are recommended to validate the findings of this study.

In conclusion, our results suggest that DFU patients with a low SEP are strongly associated with an increased rate of amputation and mortality. Hence, more attention needs to be given to such patients. Addressing SEP in patients with DFUs and providing targeted care for them may improve the prognosis.