Barriers to Diabetic Foot Management in Italy

Nutrition, Metabolism & Cardiovascular Diseases (xxxx) xxx, xxx

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Nutrition, Metabolism & Cardiovascular Diseases

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Barriers to diabetic foot management in Italy: A multicentre survey in diabetic foot centres of the Diabetic Foot Study Group of the Italian Society of Diabetes (SID) and Association of Medical Diabetologists (AMD)

Marco Meloni a,*, Silvia Acquati b, Carmelo Licciardello c, Ornella Ludovico d, Mario Sepe e, Cristiana Vermigli f, Roberto Da Ros g a Diabetic Foot Unit, Department of Systems Medicine, University of Rome Tor Vergata, Italy b Unit of Endocrinology, Pierantoni-Morgagni Hospital, Forlì AUSL Romagna, Italy c UFC Malattie disendocrine e dismetaboliche, Centro Catanese di Medicina e Chirurgia, Catania, Italy d Unit of Endocrinology, IRCCS Casa Sollievo della Sofferenza, San Giovanni Rotondo, Italy e Posturology Centre, Salerno, Italy f Unit of Endocrinology, Diabetic Foot Centre, University Hospital Santa Maria della Misericordia, Perugia, Italy g Ssd Diabetologia, Monfalcone Gorizia Asugi, Italy

Received 4 October 2020; received in revised form 12 October 2020; accepted 13 October 2020 Handling Editor: G. Targher Available online ---

KEYWORDS Abstract Background and aims: Diabetic foot (DF) disease is a current health and social burden. Diabetes; The authors aimed to identify the barriers to the DF management across Italy. Diabetic foot ulcers; Methods and results: A questionnaire was submitted to Italian centres dedicated to DF care. The Late referral; questionnaire was composed of 12 questions focused on the barriers to the DF management Limb salvage; including timing of referral, hospital management, and community follow-up. Each centre could Barriers to care answer by choosing a score from 1 to 5 for every item with the following numerical variables: 1 Z never; 2 Z rarely; 3 Z sometimes; 4 Z often; 5 Z always. Accordingly, for each item a national and regional score was reported and a comparison between regions was carried out. Na- tional and regional scores were estimated using the total score for each item as a numerator and the number of national centres included as a denominator. Among 102 centres, 99 were included and 3 were excluded due to missing data. The 99 centres belonged to 16 regions with the following distribution: Calabria 4, Campania 5, Emilia-Romagna 14, Friuli-Venezia-Giulia 4, Lazio 12, Liguria 4, Lombardy 10, Marche 1, Molise 1, Piedmont 5, Apulia 5, Sardinia 5, Sicily 4, Tuscany 11, Veneto 9, Umbria 5. The items with the highest score were late referral (3.3) and urgent surgery (3.2). The regions with the highest score were Molise (3.9) and Calabria (3.5). Conclusion: The main issues across Italy were late referral and the requirement for urgent surgery for acute DF. In the regional scenario, the southern central areas showed more barriers than northern regions. ª 2020 The Italian Diabetes Society, the Italian Society for the Study of Atherosclerosis, the Ital- ian Society of Human Nutrition and the Department of Clinical Medicine and Surgery, Federico II University. Published by Elsevier B.V. All rights reserved.

* Corresponding author. Dept. of Systems Medicine, University of Rome Tor Vergata, Via Montpellier 1, 00133 Roma, Italy. E-mail address: [email protected] (M. Meloni). https://doi.org/10.1016/j.numecd.2020.10.010 0939-4753/ª 2020 The Italian Diabetes Society, the Italian Society for the Study of Atherosclerosis, the Italian Society of Human Nutrition and the Department of Clinical Medicine and Surgery, Federico II University. Published by Elsevier B.V. All rights reserved.

Introduction Results

Although in the last number of years several improve- National barriers ments have been documented with regards to diabetic foot management, diabetic foot ulcers (DFUs) remain a Among 102 centres which responded to the questionnaire, considerable healthcare, social and economic burden [1]. 99/102 were included and 3/100 were excluded due to Despite a continuous implementation of guidelines, missing and/or incorrect data. The 99 centres belonged to as well as the organisation of specific courses and 16 regions with the following distribution: Calabria 4, meetings, the knowledge of diabetic foot disease ap- Campania 5, Emilia-Romagna 14, Friuli-Venezia-Giulia 4, pears to be less than adequate [2]. Likewise, the Lazio 12, Liguria 4, Lombardy 10, Marche 1, Molise 1, approach is often driven by a personal opinion [2,3]and Piedmont 5, Apulia 5, Sardinia 5, Sicily 4, Tuscany 11, late referral to specialised diabetic foot centres is a Veneto 9, Umbria 5. common theme [4]. Among those centres, 43 were recorded as 2nd level Furthermore, it is widely accepted that differences in diabetic foot centres and 56 as 3rd level diabetic foot health care organisation often lead to different pathways centres. of care which could influence delayed diagnosis and The items with the highest score were delayed referral treatment and negatively impact on ulcer healing and (average score 3.3), urgent surgery (3.2), elective hospi- amputation. talization (3.1) Table 1. The item with the lowest score Even though recent data put the Italian health care was the availability of prescribed foot orthotics (1.9) system among the countries with the lowest rate of major Table 1. amputation [5,6], it is a common opinion that several barriers which could influence the pathway and the management of diabetic foot are still present, both in Regional barriers hospital and community settings. The aim of this survey designed by the Italian Diabetic The regions with the highest average global score were Foot Study Group was to identify the barriers and gaps in respectively Molise (3.9) and Calabria (3.5), while Umbria the management of diabetic foot disease among Italian reported the lowest average score (1.4). Table 2. diabetic foot centres.

Delayed referral Methods This barrier was more often present in Molise, Marche, The survey was developed through a pre-set questionnaire Campania, Lazio, Calabria and Sardinia, while it was rarely which was submitted to each Italian diabetic centre present in Apulia, Piedmont and Tuscany. dedicated to diabetic foot care. The questionnaire was composed of 12 questions focused on the barriers and gaps in the management of diabetic foot. Urgent surgery Timing of referral, hospital management including both surgical and vascular aspects and follow-up in the com- This barrier was more frequently present in Molise, Apulia, munity were evaluated. Marche, Calabria, Sardinia and Lazio, while it was rarely Each centre could answer by choosing a score from 1 to present in Liguria, Tuscany and Veneto. 5 for every item analysed with the following numerical data: 1 Z never; 2 Z rarely; 3 Z sometimes; 4 Z often; 5 Z always (see the questionnaire in the supplementary Table 1 National average score for each item. material section). Item Score The questionnaire was performed by the local medical Delayed referral 3.3 team in each centre and submitted to a central database in Urgent surgery 3.2 which all questionnaires were recorded. Elective hospitalization 3.1 Accordingly, for each item, a national and regional score Length of hospitalization 2.7 was reported and a comparison between regions was Management in the community setting 2.7 carried out. Elective surgery 2.6 Hospitalization 2.4 The national score was estimated using the total score Surgical revascularization 2.3 for each item as a numerator and the number of national Post-hospitalization management (follow-up 2.2 centres included as a denominator; the regional score was management) estimated using the total score for each item as a numer- Endovascular revascularization 2.2 ator and the number of centres included for the respective Discharge 2.1 Prescription therapeutic footwear 1.9 region as a denominator.

Please cite this article as: Meloni M et al., Barriers to diabetic foot management in Italy: A multicentre survey in diabetic foot centres of the Diabetic Foot Study Group of the Italian Society of Diabetes (SID) and Association of Medical Diabetologists (AMD), Nutrition, Metabolism & Cardiovascular Diseases, https://doi.org/10.1016/j.numecd.2020.10.010 arest ibtcfo care foot diabetic to Barriers h ibtcFo td ru fteIainSceyo ibts(I)adAscaino eia ibtlgss(M) Nutrition, (AMD), Diabetologists Medical of Association and of (SID) centres foot Diabetes diabetic of in survey Society multicentre Italian A Italy: the https://doi.org/10.1016/j.numecd.2020.10.010 in Diseases, management of Cardiovascular foot Group diabetic & to Study Metabolism Barriers al., Foot et Diabetic M Meloni the as: article this cite Please

Table 2 Average score for each region. The regional scores below the mean national score for each item are highlighted in bold.

Region Delayed Urgent Elective Length of Management in the Elective Hospitalization Surgical Follow-up Endovascular Discharge Prescription referral Surgery Hospitalization hospitalisation community setting Surgery revascularization management revascularization therapeutic footwear Calabria (4) 3.7 4 3.7 3 3.7 3.5 3.7 3 3.2 3.2 3.7 3.5 Campania 3.8 2.2 2 3.2 4 2.2 1.4 1.8 3 1.2 1.6 2.4 (5) Emilia- 2.8 3.3 3.8 2.8 1.9 3 2.2 2.6 1.8 2.8 2.3 2.4 Romagna (14) Friuli- 4 2.5 3 3.2 2.2 2.2 2 2.5 2.2 2.7 3 1.7 Venezia- Giulia (4) Lazio (12) 3.8 3.7 3.2 3.2 3.9 3.2 3.2 2.8 2.8 2.3 2.5 1.5 Liguria (4) 2.7 1.7 2.5 1.7 1,7 1.7 2.2 1 1.5 1 1.5 1.2 Lombardy 3.4 2.4 2.7 2.5 2.5 1.8 2.3 1.7 2.3 1.9 2.1 2.2 (10) Marche (1) 4 4 322 33 3 22 21 Molise (1) 5 5 4 4 5 5 4 5 3 223 Piedmont 2.2 3.2 3.2 3.4 2.6 2.2 2 2.2 2 2.4 2.8 1.6 (5) Apulia (3) 2 4.6 4.6 3.3 3.6 3.6 2 3 3 3 2.6 3 Sardinia (5) 3.6 3.8 3.2 3 2.4 2.8 3 2.4 2.2 3.2 2.2 1.8 Sicily (4) 333 2.7 3.5 2.2 2.2 2.2 2.7 1.5 2 1.7 Tuscany (11) 2.3 2 2.2 2.7 2 2 2.1 1.9 1.7 1.3 1.9 1.8 Veneto (9) 3.6 2.1 2.5 1.8 2.5 1.6 2 1.7 1.6 2 1.8 1.3 Umbria (7) 2.7 3 2.3 2 2 2.1 2.1 1.7 1.4 1.9 1.3 1.7 3 4 M. Meloni et al.

Elective hospital admission Prescription therapeutic footwear

This barrier was often frequent in Apulia, Molise, Emilia- This barrier was often present in Calabria, sometimes in Romagna and Calabria, whereas it was rarely an issue in Molise, and never in Marche. Campania, Tuscany, Umbria, Veneto and Liguria. Discussion Length of hospitalization This survey is the first of its kind to investigate barriers and This barrier was often present in Molise, sometimes in gaps in the management of diabetic foot disease in Italy, Piedmont, Apulia, Campania, Friuli, Lazio, Calabria and both in hospital and community settings. Emilia-Romagna, whilst it was rarely present in Liguria, The main barriers identified across the whole national Veneto and Umbria. area were late referral to specialised diabetic foot centres, urgent surgical treatment in the case of acute diabetic foot and elective hospital admission. Management of diabetic foot disease in the community Delayed referral is a common theme worldwide, and a setting recent survey by the International Diabetic Foot Care Group (IDFCG) and D-Foot International showed that in This barrier was always present in Molise, often in Cam- four European countries (UK, Spain, Germany and France), pania, Lazio, Calabria and Sicily, while rarely was it an issue the ulcer duration was unknown in 55e65% of cases at the in Liguria, Emilia-Romagna, Tuscany, Umbria and Marche. first visit or the diagnosis was delayed for more than 3 weeks from the onset of the ulcer [4]. Elective surgery Furthermore, approximately 50% of patients were referred after 1 month following the onset of foot ulcera- This barrier was always present in Molise, often in Apulia tion, and only 40% of GPs were aware of the dedicated and Calabria, and rarely present in Veneto, Liguria, Lom- diabetic foot centres operating in their respective health bardy, Tuscany and Umbria. care areas [4]. Although in this survey the authors did not thoroughly investigate the causes of late referral, it is a shared opinion Hospitalization for diabetic foot disease that it could often be related to poor knowledge of diabetic foot disease, both for health care professionals and This barrier was more frequently present in Molise and patients. Calabria while it was uncommon in Campania. Delayed referral was a critical situation, which was more evident in Molise, Marche, Campania, Lazio, Calabria Surgical revascularization and Sardinia and rarely in Apulia, Piedmont, Tuscany and Umbria. This barrier was always present in Molise, sometimes in This difference among regions involved in the survey Sardinia, Apulia, Marche, Calabria, Lazio and Emilia- could be also related to different health care systems and fi Romagna, and never in Liguria. speci c pathways of care which may or may not allow for an early referral to specialised diabetic foot centres. This often occurs in Umbria and Tuscany, where pre-set diag- Community follow-up after hospitalization nostic and treatment pathways for patients with DFUs are available and recognised by the regional health care sys- This barrier was sometimes present in Calabria, Molise, tems [7e10]. Apulia, Campania, Lazio and Sicily, while rarely present in Delayed referral of DFUs could lead to worse outcomes Umbria, Liguria, Veneto, Tuscany, and Emilia-Romagna. in comparison to early referral, increasing the risk of non-healing as reported by a recent Audit of English and Welsh Diabetic Foot Care [11], or a reduced rate of Endovascular revascularization healing (>58%) in the case of referral after 52 days from the ulcer onset in comparison to early referral as Endovascular revascularization was a barrier which was described by Smith-Strøm et al [12]. sometimes present in Sardinia, Calabria, Apulia, Emilia- The unfavourable prognosis due to late referral can be Romagna and Friuli, and rarely in Liguria, Campania, Tus- reinforced by the waiting times for hospital elective cany and Sicily. admission, which is another major barrier reported through the survey. This condition usually concerns Hospital discharge chronic ischemic patients needing peripheral revascularization or patients with chronic DFUs needing elective Hospital discharge was often a critical issue in Calabria, surgery. It appears that the longer the ulcer duration, the while rarely did it present as a problem in Umbria and higher the risk of non-healing, infection and amputation Liguria. [13e15].

A significant critical point was the availability of urgent The study reported the results of a quantitative survey foot surgery which resulted in a barrier that was homo- and not qualitative data. The specific causes of described genously widespread across Italian diabetic foot centres, barriers were not analysed, although the aim of the au- even though it appeared to be more often present in thors was to identify gaps and critical situations in the Molise, Apulia, Marche, Calabria, Sardinia and Lazio, than management of diabetic foot, regardless of the respective in other regions. reasons. The score of every region is the average score of Urgent surgical procedures are performed in the case of the centres included and may be partially influenced by moderate/severe diabetic foot infections associated with the number of centres within each region. It would be wet gangrene, phlegmons, abscesses, necrotizing fasciitis useful in the future to analyse the same elements within or osteomyelitis involving soft tissues [16]. In the the different regional areas. mentioned above cases, surgical treatment is mandatory In conclusion, although Italy is one of the countries and should be performed usually within 24e48 h, with the lowest rate of lower limb amputation, this survey regardless of the degree of peripheral blood perfusion, to allowed the identification of some barriers influencing the avoid or limit the extent of infection and compartment management of diabetic foot disease, mainly late referral syndrome [17]. and urgent surgical treatment in the case of critical dia- This data highlights the need to educate all health care betic foot. Critical situations are more frequent in central professionals and reinforce the awareness of diabetic foot and southern areas and are rarely seen in northern disease among patients with DFUs or those at risk of regions. ulceration. This is the first study to detect the main barriers and A recent research study showed that GPs are often gaps in the management of diabetic foot disease across poorly trained in the management of diabetic foot [3] and Italy. The data reported could help clinicians to improve foot examination is uncommon [18]. Similar data were pathways, strategies and treatment of patients with dia- found in Italian research on diabetes care which showed betic foot, both in hospital and community settings. that it is unusual for the feet to be examined in diabetes It is evident that there is a need to train health care centres [19]. professionals, to develop specific care pathways to Therefore, it is evident that there is a need to increase improve early referral, to have operating rooms available awareness on the management of DFUs among less trained for urgent surgery, dedicated beds and vascular operating professionals and to identify specific pathways of care for rooms for revascularization procedures as well as specific patients with diabetic foot. In addition, professionals pathways in the community for patient management after involved in primary care should perform the initial inter- hospitalization. vention and identify the timing of referral for each case, according to ulcer severity. Ethical statement A positive piece of data was that barriers to prescribed foot orthotics were found to be rare among diabetic foot The study protocol was approved by the Società Italiana di specialists, except in the regions of Calabria and Molise. Diabetologia (SID) and Associazione Medici Diabetologici This achievement is a strength, mainly in secondary pre- (AMD). vention where it has been reported that therapeutic footwear can reduce ulcer recurrence [20e22]. The availability Declaration of competing interest of prescription orthotic footwear is usually safeguarded by the Italian health care system who define diabetes and its The authors declares that there is no conflict of interest. long-term complications as a “protected disease” and allow for free prescription foot orthotics for patients in secondary prevention [23]. Appendix A. 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