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 Table of Contents  
Year : 2022  |  Volume : 1  |  Issue : 2  |  Page : 114-120

Epidemiology of infections in diabetes, pre and post-COVID era in India

Department of Endocrinology, IMS and SUM Medical College and Hospital, Bhubaneswar, Odisha, India

Date of Submission19-Apr-2022
Date of Decision03-Jun-2022
Date of Acceptance16-Jun-2022
Date of Web Publication16-Jul-2022

Correspondence Address:
Jayshree Swain
Department of Endocrinology, IMS and SUM Medical College and Hospital, Bhubaneswar - 751 003, Odisha
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/cdrp.cdrp_7_22

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Infectious diseases are more common and severe in diabetes. Diabetes predisposes to various infections through alterations in innate and acquired immune defences. Outcomes of infection are worse in people with uncontrolled glycemia, including an increased mortality. The infections can affect all organs and all systems. In patients with diabetes, the infections can be broadly classified into two categories. Infections that are common in the general population have more severe clinical presentation and worse outcomes among patients with diabetes. The second group is of infections that are peculiar to patients with diabetes, being virtually rare in the normal population, such as foot infections, malignant external otitis, rhinocerebral mucormycosis, emphysematous pyelonephritis and gangrenous cholecystitis, etc. Epidemiological data on the true incidence of atypical and rare infections are scarce. This review will highlight the prevalence, consequences, severity, and pattern of infections in the population with diabetes in India. This review of epidemiological prevalence may guide the clinicians for early suspicion, identification of infectious disease, and right selection of the antimicrobial agents which may lead to a better outcome.

Keywords: Diabetes, epidemiological data, immunity, infections, prevalence

How to cite this article:
Swain J, Singh J, Manglunia A, Jena S, Sravya S L. Epidemiology of infections in diabetes, pre and post-COVID era in India. Chron Diabetes Res Pract 2022;1:114-20

How to cite this URL:
Swain J, Singh J, Manglunia A, Jena S, Sravya S L. Epidemiology of infections in diabetes, pre and post-COVID era in India. Chron Diabetes Res Pract [serial online] 2022 [cited 2023 Mar 29];1:114-20. Available from: https://cdrpj.org//text.asp?2022/1/2/114/351260

  Introduction Top

The relationship between infection and diabetes is bidirectional. People with diabetes are more prone to infections and that too associated with higher complications, as compared to individuals without diabetes. Infections per se can lead to hyperglycemia due to cytokine surge. These cytokines interfere with insulin signaling mechanisms leading to a state of insulin resistance, thereby leading to hyperglycemia. It is one of the leading causes of morbidity and mortality in people with diabetes, especially in developing parts of the world, where diabetes is generally recognized during work-up for infections.

The COVID-19 pandemic has spread from its epicenter in Wuhan, China since December 2019 to infect over 86 million people with over 1.8 million deaths in 222 countries worldwide till January 2021. COVID-19 is associated with more severe outcomes in diabetes.[1] Moreover, with the use of empirical antibiotics and steroids for the treatment of COVID-19, there is an increase in antibiotic resistance as well as increase incidence of infections with atypical organisms, which is more in the case of diabetes.[1]

Actual incidence of infections in diabetes is difficult to determine, but few infections are predominantly seen in people with diabetes. Such infections include malignant otitis externa, mucormycosis, emphysematous forms of cholecystitis, cystitis and pyelonephritis, necrotizing fasciitis, and Fournier gangrene, etc.

This review highlights the prevalence, characteristics, consequences, and etiological agents implicated in the infections among people with diabetes in India during the pre and post-COVID period along with the mechanisms how immunity is affected in diabetes.

  Diabetes and Immunity Top

Diabetes impairs both the adaptive immune response and innate immunity. The increased susceptibility to infections in diabetes is explained by impaired humoral and cell-mediated immunity. In humoral immunity, there is impaired cytokine production of Interleukin (IL-1) β, IL-6, interferon-gamma and tumor necrosis factor-alpha. These cytokines are important in T-cell activation which drives the cell mediated immunity. There is also a defect in Toll-like receptor expression in people with diabetes that impair the recognition of the pathogens by T-cells.[2] There is also defect in T-cell response in diabetes. All these interrupt both humoral and cell-mediated immunity.

Regarding innate immune mechanisms, there is neutrophil dysfunction in the form of defective chemotaxis, adhesion, rolling, and diapedesis. Hyperglycemia inhibits Glucose 6 Phosphate Dehydrogenase resulting in decreased nicotinamide adenine dinucleotide phosphate available for reactive oxygen species formation. This leads to impaired oxidative burst of neutrophils against the pathogen. Hyperglycemia also impairs neutrophil degranulation, decreases immunoglobulin-mediated opsonization, and impairs neutrophil extracellular trap formation.[3]

Macrophage function too is impaired in hyperglycemia. Complement receptor defects were seen on the monocytes in chronic hyperglycemia resulting in phagocytic defects.[4] Hyperglycemia causes macrophage polarisation that shifts to M2-macrophages, having poor microbicidal activity and thus weakens the immunity.[5] Diabetes also causes natural killer cell dysfunction which impairs the innate immunity of the individual. There is also inhibition of complement activation via classical or lectin pathways. As a result of this, there is an increase in the propensity to infections.

  Diabetes, Infection and Mortality Top

As per the 10th edition of International Diabetes Federation Diabetes  Atlas More Details, 6.7 million deaths were attributable to diabetes in 2021, which accounts for 12.2% deaths from all causes. 32.6% of these deaths were in adults <60 years of age.[6]

A retrospective cohort study in 1999 in Canada compared patients with diabetes with matched control subjects without diabetes. Among the diabetes group analysis, 46% of subjects developed infections of which few required even admission compared to nondiabetes group. The mortality risk-ratio was also significantly higher in the diabetes group.[7]

Indian mortality data too suggests higher mortality among people with diabetes due to infections. According to the Chennai Urban Population (epidemiological) Study in South India 16 study, the diabetic cohort had a three-fold higher mortality (18.9/1000 person years) compared to normoglycemic people (5.3/1000 person years P = 0.004).[8] Bhansali et al., (hospital-based retrospective study in North India) revealed infections as a major contributor of mortality in diabetes (46.5%) followed by coronary artery disease and renal failure.[9] Similarly, a study by Zargar et al. in Kashmir valley too reported that infections was the major contributory factor for mortality among 40.9% of people with diabetes. Among these patients, infection was the sole factor responsible for mortality in 10.7% of cases.[10],[11] Infections were the leading cause of mortality followed by chronic kidney disease (30.85%) and cardiac disease (16.3%).[10] An Eastern India study from Odisha (1991) concluded that infection was the second most common cause of mortality (33.7%) after chronic kidney disease (35%).[12] However, a recent prospective hospital-based study from the same center showed that infections were also the second most common cause of death (27.3%) after cardiovascular-related death (51.5%).[13] The mortality trends in diabetes in developing regions somehow differ from that of developed regions in most of the studies. In Western countries, coronary artery disease and cerebrovascular disease are leading causes, whereas infections and chronic renal failure in India.

  Diabetes and Spectrum of Infection Top

Various studies have shown that the urinary and the lower respiratory tract, mucous membrane and skin are the common sites of infection in diabetes in the community and surgical wound infection in hospital-acquired cases.[14]

Profile of infections in Type 2 diabetes mellitus in a study from Eastern India revealed that urinary tract infection was 31.8%, pneumonia was 30.3%, septicemia 30.3%, malaria 06%, enteric fever 06%, diabetic foot 4.5%, and tuberculosis (TB) 4.5%.[15] Common infections encountered in a study from a rural tertiary care hospital of South India were: upper respiratory tract infections (29.13%), urinary tract infections (UTI) (26.17%), lower respiratory tract infections (LRTI) (15.74%), and pulmonary Koch's (11.81%). Balanoposthitis, periodontitis, vaginitis, amebic liver abscess, infective endocarditis, etc., too are commonly seen in diabetes.[16] In a study from a tertiary care center of North India, most common infections encountered were soft tissue (42.8%), respiratory tract (30.2%), and genitourinary tract (GUT) (28.5%). In 5.3% cases, infection of more than one site was found.[17]

Genitourinary tract

GUT infection is commonly seen in diabetes. This includes urethritis, cystitis, prostatitis, and vaginitis in females. UTI risk is increased by 60% and genital tract infections rise by two-four fold in diabetes.[18] Among people with diabetes, UTI is often bilateral, involves upper urinary tract (80% cases) and is more likely to develop complications.[14] Furthermore, recurrence of this infection (25%–45%) is significantly higher compared to people without diabetes.[19] The risk of hospitalization is increased by two folds due to the recurrent nature of the diseases and complications association with UTI, as compared to the people without diabetes.[20]

Majority of the Indian people with diabetes with UTI and positive cultures are asymptomatic (30%).  Escherichia More Details coli (64.6%), Klebsiella (12.1%) and Enterococcus (9.9%) are the most detected organisms. Extended-spectrum beta-lactamase producing E. coli variety is detected more in diabetes. Higher prevalence of pyelonephritis is seen among people with diabetes with uncontrolled hyperglycemia.[20] In a study, among 495 people with diabetes with UTI, 533 pathogens were isolated of which Gram-negative and Gram-positive cocci were 362 and 100, respectively, whereas, in 71, the pathogen isolated was Candida.[21] E. coli was the most common organism isolated (71%) amongst Gram-negative cocci, followed by Pseudomonas (8%) and Proteus (1%). As far as Gram-positive cocci are concerned, enterococci were most seen with 59% prevalence, Staphylococcus aureus Scientific Name Search  (coagulase negative) is 25%, beta hemolytic streptococci 8%. Candida species was seen in 80% and Candida albicans in 20% among Candida species.[21] Few other Indian studies too revealed similar uropathogens.[22],[23]

A study from Odisha too showed E. coli (61.8%) as the most common organism followed by S. aureus (14%), whereas 19.4% subjects had sterile culture.[13] Sridhar et al. in their study among menopausal diabetic women found 14% subjects with symptomatic UTI.[24] Studies from South India, too found the highest prevalence of E. coli organism among UTI. The prevalence of UTI was 26.8% in the study of Bettegowda et al. with highest pathogen prevalence of E. coli followed by C. albicans. Another South Indian study by Janifer et al. reported higher UTI prevalence (42.8%) with E. coli as the most common organism and 24.3% had sterile culture.[21] Study from a metropolitan city showed that the lower socioeconomic cohort of people with diabetes had higher UTI proportions. Pyelonephritis had 15-fold higher hospitalization rate among people with diabetes. As far as lower socioeconomic strata are concerned, prevalence of UTI was found to be 56.4% among diabetes group compared to 43.6% in normoglycemic population. Whereas amongst higher socioeconomic category, 51.6% people with diabetes and 48.4% people without diabetes had UTI. Again E. coli was the most common UTI pathogen in the Type 1 diabetes subgroup.[25]

There is an alarming increase in antibiotic resistance all over the world. A study from South India carried out on outpatient department basis found that fluoroquinolones, the most commonly used antibiotics for uncomplicated UTI, had 74% resistance.[23] Indian cohort of women with diabetes with genital infections had vulvo-vaginal candidiasis as most common infection, whereas among uncircumcised men with diabetes, Candida balanitis was most common.[26]

After the emergence of sodium-glucose cotransporter 2 (SGLT-2) inhibitors in the field of diabetic management, the risk of mycotic genital infections has increased.[27] Although there is mild-moderate severity of infection from SGLT-2 inhibitors, it responds to conventional therapy.[27] Cystitis and upper UTI are rarely found.[28]

Respiratory tract infection

LRTI in people with diabetes follow a more serious course with a longer duration of illness and a complication rate.[29] The mortality due to LRTI is also increased in people with diabetes up to four-fold higher than the general population. The prevalence of TB is increased with more complication rates and mortality. The chances of reactivation of old tubercular lesions are also increased.[30]

The course of pneumonia, TB, fungal as well as parasitic infections follow a different course in people with diabetes, with delayed resolution and recurrent respiratory tract infections. The most common organisms involved in respiratory tract infections in diabetes are S. aureus, Mycobacterium tuberculosis, Streptococcus, Legionella and Mucor infections as well as Gram-negative bacteria such as Klebsiella pneumoniae. The morbidity and mortality in these infections as compared to the general population are increased in diabetes. Previous Indian studies reported the prevalence of pneumonia in diabetes to be 11.6%[24] and 4.4%.[31] However, in a recent study from Cuttack, the prevalence was around 30.3%.

In a study from South India, the common infections encountered in diabetes were upper respiratory tract infection (29.13%) followed by UTI, lower respiratory tract infection (15.74%), and TB (11.02%).[31] The most common organisms implicated in respiratory infections were S. aureus (20%) K. pneumoniae (11.42%), and Streptococcus pneumoniae (11.42%). No organism was found in 40% cases.[31] Common causative organisms found in a hospital-based study were acid-fast bacillus 32%, streptococcus species 30%, Klebsiella and other Gram-negative 6%, atypical and fungal 18%, and polymicrobial 10%.[32]

The main risk factors for developing respiratory tract infections were age >50 years, diabetes duration of 4 years or more, and uncontrolled glycemia.[33] Males are more predisposed to diabetes with pneumonia, which is also seen in Indian studies.[32],[33] The most common age group affected in these studies was 40–60 years' age group (62%), with most of the patients from rural areas and lower socioeconomic status.[32],[33]

A study by Patel found TB to be the most common associated illness (5.9%) with diabetes.[29] In another series, the frequency of TB was found to be 4.5%.[4] Earlier studies done in people with diabetes by Bhatia, (1975) Bahulkar (1975), Nanda and Tripathy (1968) found prevalence of TB to be 14%, 4.5%, and 12%, respectively.[34] M. tuberculosis was the most common isolated pathogen found in 44% of diabetes patients in a hospital-based study.[32]

Diabetic foot infection

Diabetic foot infections (DFI) are the major cause of morbidity and mortality in people with diabetes along with increased cost of therapy and amputation. DFI contributes to amputation in 90% of the patients.[35] Among the hospitalized patients, DFI-related sepsis is the second most common cause of infection-related mortality (8.3%).[9] The socio-epidemiology of diabetic foot ulcer in India is different compared to the Western world. In the West, there are predominantly neurovascular ulcers as compared to chronic, neuropathic ulcers in India.

The frequency of diabetic foot is around 6%–11% in diabetic population. Most of these cases are attributed to diabetic neuropathy.[36] In a study by Pendsey, the prevalence of foot ulcers in patients with diabetes in clinic was 3%.[37] Similarly, in a study from Cuttack, DFI was present in 4.5% of the people with diabetes.[13]

Looking at the organisms in DFI, Gram-negative bacteria species, Pseudomonas aeruginosa is the most common isolated organism.[38] Similarly, a prospective trial in 62 consecutive subjects showed that 32% subjects had mono-microbial infections while around 35% had poly-microbial cultures. Twenty-one percentage of the subjects had no growth on culture.[39] Out of the cultured bacteria, 68% bacteria were Gram-negative, whereas 32% were Gram-positive. The most common isolated organism was E. coli with sensitivity to piperacillin/tazobactam. Similar results were found in another study where Gram-negative bacteria were commonly isolated in diabetic ulcers, in contrast to Gram-positive bacteria in nondiabetic ulcers.[40] Moreover, it was seen that 65%–80% of the people with diabetes in studies from India were not following any foot care maneuvers, despite having foot at risk.

Skin and mucous membrane

There is an increased risk of folliculitis, furunculosis, and subcutaneous abscesses in the people with diabetes. These infections appear to increase in patients with poor glycemic status. These infections may present as the first sign of diabetes or gradually appear within the course of diabetes.[41] The natural history of these infections follows a severe course in diabetes.[41]

The risk factors for skin infections in diabetes are sensory neuropathy, atherosclerotic vascular disease, and hyperglycemia. These infections mainly involve the feet, although they can involve any skin surface.[42] Recent studies found a prevalence of skin infections ranging from 20% to 50% in people with diabetes.[43] On the skin surface, fungal infections were more common than bacterial or viral infections.[44] The commonly involved sites are inter-digital spaces, genitalia, and skin folds.

In a study from South India, 11.02% patients with diabetes had skin infections. The most common infection was fungal infection followed by bacterial.[31] Similar results were reported by Foss, et al. outside India.[45] Another observational study in a tertiary care hospital revealed that 75.61% of patients with Type 2 diabetes had skin lesions as compared to 41% Type 1 diabetes patients. Infections were responsible for majority of skin lesions in Type 2 diabetes, whereas diabetic xerosis followed by infections was found in the majority of patients with Type 1 diabetes.[46]

The incidence of fungal infections, both systemic and localized is increased in diabetes. The incidence of opportunistic fungal infections such as invasive candidiasis, aspergillosis, and zygomycosis is also increased. Invasive zygomycosis is one of the infections particularly found in uncontrolled patients with diabetes in the Indian subcontinent.[47]

In critically ill patients, nosocomial blood infection with Candida is very frequent. In a retrospective study among intensive care unit (ICU) patients presenting with candidemia, diabetes was responsible for 50% of cases of Candida glabrata.[48] In a tertiary care center, mucormycosis was found in 38 patients over a 12-month follow-up period and more than 50% of rhino-orbito-cerebral mucormycosis patients had diabetes.[49]

Gastrointestinal infection

Hepatitis C was found in 11 (5.7%) out of 197 subjects with even more prevalence in men with diabetes and individuals with poor glycemic control.[50] The prevalence was slightly higher than the global prevalence in the general population which is about 3%. The prevalence of hepatitis B (58.3%) was found to be higher in patients with diabetes with acute viral hepatitis as compared with patients not having diabetes (25.3%). Even the incidence of severe hepatitis is increased in patients with diabetes (41.67% vs. 10.64%) as well as the incidence of complications such as liver failure and death.[51] Other gastrointestinal infections infections such as Helicobacter pylori were more common in patients with diabetes (77.5%) as compared to controls (58.3%). H. Pylori infections in diabetes were positively correlated with poorer glycemic control and low socioeconomic status.[52]

In the post-COVID era, the data on the epidemiology of infections in diabetes are lacking. There is an increasing number of atypical infections recognized in the post-COVID period. The incidence of infections in pre-COVID era, as discussed above, has increased in severity along with antibiotic resistance in post-COVID period. There is an increased incidence of mucormycosis in diabetes patients affected with COVID-19.[53] Mortality in mucormycosis is very high during COVID (30.7%). Out of 82 published cases of mucormycosis found in India during the COVID period, 80% of individuals had preexisting diabetes and diabetic ketoacidosis was present in 14.9% of cases. In these cases, nose and sinuses were most commonly involved in 88.9% of patients, followed by rhino-orbital area. (56.7%).[54] COVID-19 also leads to immune dysregulation, with decrease in T-lymphocytes, CD4+ T, and CD8+ T cells, further reducing innate immunity. The other thing implicated is the increased usage of steroids. In one case series reported from New Delhi, 15 patients admitted in the ICU with COVID-19 infection developed superimposed Candida infections.[55] Out of these 15 patients, 10 developed Candida auris infection and six patients had preexisting diabetes. The patients infected with C. auris infection had worse outcome and six out of 10 patients died.

  Conclusion Top

In India, the burden and pattern of infections in diabetes varies as compared to western world. Both the incidence and severity of infections has increased during the pandemic. Various aspects such as nonadherence to antidiabetic treatment, noncompliance to prescribed dose and duration of antibiotics, infrequent follow-up, leads to recurrent and resistant infections and treatment failure. Patients with diabetes have dysregulated immune response to the pathogens. Hyperglycemia further worsens the outcome. Infection is one of the major causes of death among patients with diabetes. Hence, in addition to microvascular and macrovascular complications, physicians should consider infection as a complication of diabetes at the same level. Prevention and timely intervention of diabetic infections should also be considered as a part of the national health programme.

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