Original paper Videosurgery. Łukasz Kaska, Monika Proczko, Jarek Kobiela, Tomasz Jerzy Stefaniak, Zbigniew Śledziński

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1 Original aer Videosurgery Dynamics of tye 2 diabetes mellitus laboratory remission after Roux-en-Y gastric byass in atients with body mass index lower than 35 kg/m 2 and higher than 35 kg/m 2 in a 3-year observation eriod Łukasz Kaska, Monika Proczko, Jarek Kobiela, Tomasz Jerzy Stefaniak, Zbigniew Śledziński Deartment of General, Endocrine and Translant Surgery, Medical University of Gdansk, Gdansk, Poland Abstract Videosurgery Miniinv 2014; 9 (4): DOI: /wiitm Introduction: Bariatric surgery as treatment of tye 2 diabetes mellitus (T2DM) in morbidly obese atients is becoming common. Although a large number of studies demonstrating high efficacy of bariatric methods in diabetics with body mass index (BMI) < 35 kg/m 2 have been ublished, this romising solution is still not acceted enough even in the era of a diabetes offensive. Aim: To analyze the dynamics of T2DM remission in atients with kg/m 2 and > 35 kg/m 2 after Roux-en-Y gastric byass (RYGB). Material and methods: Data of 30 atients with kg/m 2 and 82 with who underwent RYGB between 2007 and 2010 were collected from a rosectively designed database. The laboratory resolution of T2DM was determined by fasting lasma glucose (FPG 100 mg/dl) and glycosylated hemoglobin (HbA 1c 6%). Results: The T2DM regression was observed in 80% of the atients with kg/m 2 and 83% in a grou with 1 year after RYGB and about 80% 2 and 3 years after the oeration in both grous. Normalization of average HbA 1c and FPG was observed in the grou after 3 months, while in the kg/m 2 grou it was reached 6 months ostoeratively. Changes in main markers of T2DM were arallel with the BMI decrease 3 12 months after RYGB, but early resolution in some atients was observed indeendently of weight loss. Conclusions: The mid-term observation of atients after RYGB revealed the laboratory remission of T2DM. Ultimate evaluation of T2DM markers 3 years after surgery demonstrates high effectiveness of RYGB in managing T2DM in both grous. Key words: tye 2 diabetes mellitus, remission, Roux-en-Y gastric byass, surgical treatment, body mass index below 35 kg/m 2. Introduction Tye 2 diabetes mellitus (T2DM) has been recognized as one of the leading lagues of the modern world. While in 1995, there were 135 million eole affected by this disease, the aroximate rognosis for 2030 seems to be devastating the number of atients suffering from T2DM is exected to be nearly triled [1, 2]. In develoed countries, diabetes is now the fourth leading cause of death [2]. Tye 2 diabetes mellitus is the main medical condition in eole with chronic renal failure [2]. It was estimated that more than 2.5 million individuals develoed diabetic retinoathy [2]. In Poland alone, annually, about atients undergo distal lower limb amutations annually due to diabetes-related micro-angioathy [3]. Peole with T2DM are more than twice as likely to have a heart attack or stroke comared to non-diabetics [1, 2]. Estimated global healthcare exenditures to treat and revent diabetes and its Address for corresondence Łukasz Kaska MD, PhD, Deartment of General, Endocrine and Translant Surgery, Medical University of Gdansk, 17 A Smoluchowskiego St, Gdansk, Poland, hone: , lukasz.kaska@w.l 523

2 Łukasz Kaska, Monika Proczko, Jarek Kobiela, Tomasz Jerzy Stefaniak, Zbigniew Śledziński comlications are rojected to exceed USD 490 billion by the year 2030 [1, 2, 4]. These alarming data call for more intensive diabetes management and encourage the search for new alternatives to current sub-effective theraies [5]. The observation of the ostoerative course of bariatric atients with concomitant T2DM demonstrated a very high rate of long lasting resolution of tye 2 diabetes already in the late nineties [6, 7]. What was recognized as otentially curative for athologically obese diabetics could also be beneficial for atients with mild obesity or even overweight, ineffectively treated for T2DM [8]. In March 2011 during the 2 nd Congress on Interventional Theraies for T2DM in 2011 in New York, a multidiscilinary team of reutable secialists develoed an agenda of research riorities to set a new consensus on the role of gastrointestinal surgery in T2DM treatment in obese and non-obese atients [9]. Since the results of the two most imortant randomized trials comaring conservative with surgical treatment of T2DM were ublished in 2012, the number of bariatric rocedures for diabetic atients with different body mass index (BMI) has increased worldwide [8 11]. Aim The aim of the study was to evaluate the imact of Roux-en-Y gastric byass(rygb) on diabetes resolution in atients with BMI < and > 35 kg/m 2 in a 3-year observation eriod. We attemted to define the dynamics of change of the main diabetic laboratory markers glycated hemoglobin (HbA 1c ) and fasting lasma glucose (FPG) during weight loss following surgery. Material and methods Data of 112 atients with T2DM who underwent RYGB between Setember 2007 and December 2010 were collected in a rosectively designed database. Eighty-two of them had BMI higher than 35 kg/m 2 (mean BMI = 44.2 kg/m 2 ), and 30 had BMI lower than 35 kg/m 2 (mean BMI = 29.1 kg/m 2 ). The BMI value was calculated during the initial visit. Patients were followed u 3, 6, 12, 24 and 36 months ostoeratively. There were 21 women and 9 men in the grou with kg/m 2 and 50 women and 32 men in the grou with. The rocedure of RYGB was chosen for all of the atients because of its otential curative metabolic effect in T2DM. Diabetic atients with BMI lower than 35 kg/m 2 were referred for surgery by diabetologists due to ineffective conservative treatment of T2DM, while the dominant indication in grou was obesity. The indication criteria for RYGB for morbidly obese individuals are well established worldwide [12]. The conditions that should be met to select atients below 35 kg/m 2 BMI for surgical treatment within a clinical study are listed in Table I, following the IDF statement [13]. The reoerative eriod lasted 3 4 months and was based on cooeration with a sychologist, dietician, diabetologist and bariatric surgeons. During this eriod at least 2 visits with each of the secialists were obligatory to otimize general conditions of the atients at the time of surgery and reare them to follow the ostoerative dietary indications. At each follow-u oint aart from the BMI, the most significant markers of glycemia control acknowledged by leading diabetes associations were assessed glycosylated hemoglobin (HbA 1c %) and fasting lasma glucose (FPG mg%) [14]. In all cases, the reoerative HbA 1c and FPG were determined. In addition, the tye and dose of the antidiabetic drugs and the duration of the disease were noted. HbA 1c and FPG levels were measured 3, 6, 12, 24 and 36 months after the surgery. Many other laboratory arameters were estimated regularly after the oera- Table I. Inclusion/exclusion criteria for atients with kg/m 2 Inclusion criteria Unregulated T2DM HbA 1c > 7% (3 3 months) ΔFPG > 250 mg% C-etide > 1 ng Duration of disease > 15 years Multi-discilinary team aroval Exclusion criteria Uncontrolled sychiatric disease Age < 18 and > 65 years Alcohol or drug abuse Anti-GAD (+) GI inflammatory diseases Pregnancy Cancer history > 5 years Renal, liver failure Serious cardiovascular comlications 524

3 Dynamics of tye 2 diabetes mellitus laboratory remission after Roux-en-Y gastric byass in atients with body mass index lower than 35 kg/m 2 and higher than 35 kg/m 2 in a 3-year observation eriod tion to estimate the efficacy of the treatment and revent nutritional deficiencies, but have not been resented here not to blur the basic idea of the study. All atients underwent RYGB. Sixty-five of them underwent a laaroscoic rocedure (LRYGB) and 47 an oen rocedure (ORYGB). Regardless of the aroach, the technical asects of the rocedures were the same. The size of the ouch was measured during the obligatory methylene blue test and ranged from 35 ml to 45 ml. Intestinal anastomosis was erformed after the exclusion of bilioancreatic limb (BPL) average 109 cm with digestive limb (DL) 154 cm in the grou, and the roortion BPL/DL in the kg/m 2 grou was close to the average of 100/100 cm. The size of the limbs was adjusted to the BMI of the atients with BMI > 35 kg/m 2 but in some cases the anatomical conditions layed the deciding role. Hence the main goal in kg/m 2 atients was not intense weight loss, and the length of both loos was set at about 100 cm. The follow-u visits were executed by a multidiscilinary team at the above-mentioned time oints. The glycemia markers were all assessed in the same laboratory. The National Institutes of Health (NIH) guidelines define normal FPG as 100 mg% and the nondiabetic range of HbA 1c as % [15]. The laboratory T2DM remission has been established following NIH criteria for atients who discontinued using diabetic medications. Grou characteristics are summarized in Table II. The sectrum, methodology and assumtions of the study were acceted by a local bioethical committee at the Medical University of Gdansk, Poland. Statistical analysis Statistical analysis was erformed with Statistica software licensed for the Medical University of Gdansk. Data at individual time oints were comared using t-tests. Statistical significance was considered for < Results All 112 atients were followed u according to the schedule of the study. There were no intra- or ostoerative deaths. Gastrointestinal leak as the most serious comlication was observed in 2 atients from the grou. The first leak was localized in the site of the stale line of the remnant stomach. It required reoeration and closure on the second ostoerative day. The stenosis of the ouch-jejunal anastomosis 12 months after the rocedure was the reason of late ouch cutaneous fistula in another case. Endoscoic dilatation of the anastomosis with self-exanding stent imlantation and intense arenteral nutrition for 6 weeks was safe and effective in fistula closure. Control endoscoy 1 year after RYGB showed ulceration in the region of anastomosis in 6% to 10% of atients in both grous, which were successfully treated conservatively. All the ostoerative comlications and the most common adverse Table II. Grou characteristics Base conditions kg/m 2 Value of Number of cases Male/female 9/21 32/50 Average age [years] 46.4 ± ± Patients on insulin theray [%] Average disease duration [years] 7.9 ± ± Average HbA 1c [%] 8.9 ± ± Average FPG [mg%] 199 ± ± Average C-etide level [μg/l] 1.9 ± ± Average BMI [kg/m 2 ] 29.1 ± ±5.49 < Mean size of ouch [ml] 45 ± ± Average length of BP/digestive loo [cm] 98.4/105.9 ±12.53/ /154.2 ±13.19/ / <

4 Łukasz Kaska, Monika Proczko, Jarek Kobiela, Tomasz Jerzy Stefaniak, Zbigniew Śledziński Table III. Adverse events and comlications BMI Variables BMI < 35 kg/m 2 > 35 kg/m 2 Number of cases Gastrointestinal leak or fistula 0/30 2/82 (2.4%) Anastomotic stenosis 1/30 1/82 (1.2%) Ulceration in anastomosis 3/30 (10%) 5/82 (6.1%) Wound infection 1/30 (3%) 4/82 (4.9%) Incisional hernia 0/30 2/82 (2.4%) Anemia Hb < 10 g% 0/30 2/82 (2.4%) Pneumonia 0/30 1/82 (1.2%) Hyoglycemic eisode 12/30 (40%) 31/82 (37.8%) Reoeration 0/30 3/82 (3.6%)^ Endoscoic intervention 1/30 (3%) 2/82 (2.4%) Intens. conservative treatm. 1/30 (3%)* 2/82 (2.4%)*,# Extensive vomiting 0/30 1/82 (1.2%) Duming 1/30 (3%) 6/82 (7.3%) Reflux symtoms 0/30 1/82 (1.2%) Prolonged diarrhea 0/30 4/82 (4.9%) Malnutrition 0/30 1/82 (1.2%) # *Patients exerienced symtomatic hyoglycemia eisode with glucose level < 50 mg/dl and required iv fluid administration and diet correction during 1-day hosital stay; # 1 atient required re-hositalization and arenteral and enteral feeding due to symtomatic hyoroteinemia. ^One reoeration due to leak, 2 due to incisional hernia events reorted during the ostoerative follow-u visits are listed in Table III. About 40% of the atients in both grous reorted clinical symtoms of hyoglycemic eisodes but in Table IV. Glycated hemoglobin (HbA 1c ) change only 2 atients who required intensive medical treatment accidental lasma glucose was below 50 mg%. The laboratory regression of T2DM based on HbA 1c during the first follow-u visit (3 months after surgery) was observed in 27% of the kg/m 2 grou and in 52% of the grou ( = ). In the vast majority of these atients an FPG level lower than 100 mg% was observed during the hosital stay after surgery. The average HbA 1c during the first follow-u visit was 6.1% and 6.0% in the grou with BMI < 35 kg/m 2 and the grou with resectively ( = 0.362). The decrease of the FPG from the baseline was statistically more significant in the grou of atients with : 17% 50% of the cases ( = 0.028). A further decrease in both arameters was observed in both grous at the next follow-u visit 6 months after surgery; statistically significant differences were noted between grous. At this oint laboratory regression of T2DM was observed in close to 80% of atients from the grou, while still 13/90 (43%) atients from the kg/ m 2 grou had HbA 1c higher than 6%. Delayed imrovement in HbA 1c in relation to FPG seems to reflect the fact that it illustrates glycemia control from revious weeks, rather than the current status as FPG. The values of HbA 1c and FPG at the next follow-u visits, 1, 2 and 3 years ostoeratively, demonstrated further decrease or stabilization and did not differ between the studied grous. About 80% of all cases resented HbA 1c and FPG below or equal to the threshold established as non-diabetic. The average of HbA 1c and FPG in both grous did not differ significantly in the two final follow-u visits. The values of the above-mentioned arameters are detailed in Tables IV VI. HbA 1c %Δ HbA 1c kg/m 2 SD kg/m 2 Base kg/m 2 SD kg/m 2 3 M M < < M M M

5 Dynamics of tye 2 diabetes mellitus laboratory remission after Roux-en-Y gastric byass in atients with body mass index lower than 35 kg/m 2 and higher than 35 kg/m 2 in a 3-year observation eriod Table V. Fasting lasma glucose (FPG) change kg/m 2 SD kg/m 2 Base FPG %Δ FPG kg/m 2 SD kg/m 2 3 M M < M M M Table VI. Percentage of atients in laboratory T2DM remission FPG < 100 mg% > 35 BMI > 35 BMI > 35 BMI > 35 BMI > 35 3 months 6 months 12 months 24 months 36 months BMI kg/m 2 kg/m 2 kg/m 2 kg/m 2 kg/m 2 kg/m 2 kg/m 2 kg/m 2 kg/m 2 kg/m 2 5/30 (16.6%) 41/82 (50%) 15/30 (50%) 65/82 (79.3%) 24/30 (80%) 68/82 (82.9%) 23/30 (76.6%) 64/82 (78.1%) 23/30 (76.6%) t-test HbA 1c < 6% 8/30 (26.7%) 43/82 (52%) 17/30 (56.7%) 66/82 (81%) 24/30 (80%) 68/82 (82.9%) 24/30 (80%) 66/82 (80.5%) 24/30 (80%) t-test /82 (78.1%) 64/82 (78.1%) Table VII. Body mass index (BMI) change kg/m 2 SD kg/m 2 Base < BMI %Δ BMI kg/m 2 SD kg/m 2 3 M < < M < < M < < M < < M < < The dynamics of change in both diabetic markers observed in all atients after RYGB aralleled the rogress in change of BMI. More severe BMI reduction was obviously observed in the grou of individuals with morbid obesity. None of treated atients reached the BMI delimited for the underweight (Table VII). The dynamics of change in the investigated arameters are shown in Figures 1 3. Discussion Tye 2 diabetes mellitus is suosed to be the most raidly exanding disease worldwide that sig- 527

6 Łukasz Kaska, Monika Proczko, Jarek Kobiela, Tomasz Jerzy Stefaniak, Zbigniew Śledziński Base 3 M 6 M 12 M 24 M 36 M kg/m 2 Figure 1. Dynamics of HbA 1c change Base 3 M 6 M 12 M 24 M 36 M kg/m 2 Figure 2. Dynamics of FPG change Base 3 M 6 M 12 M 24 M 36 M kg/m 2 Figure 3. Body mass index (BMI) evolution nificantly imacts morbidity and mortality [2]. Currently aroximately 250 million affected individuals require tight glycemic control to minimize the risk of consequences of macro- and microvascular changes [16, 17]. That number is exected to extend to nearly 300 million in the next 20 years [1, 2]. Moreover, in the general oulation the lifetime risk of develoing T2DM is redicted to rise to 20% [2]. Desite intense research in harmacology and introduction of advanced multi-agent management, a large number of atients cannot be otimally treated [5, 9, 18, 19]. Furthermore, T2DM is usually considered a relentless chronic and rogressive disease because harmacological treatment cannot ensure a cure, but only a delay in the develoment of its consequences. The alarming rognosis necessitates the search for more effective anti-diabetic treatment and the introduction of new, romising methods into international guidelines to offer otentially comlete remission [20]. A significant amount of evidence demonstrates that bariatric oerations, articularly methods byassing the duodenum and art of the jejunum such as gastric byass (RYGB) and bilioancreatic diversion (BPD), raidly and significantly ameliorate T2DM, leading to remission of disease in a majority of cases. These observations are not limited to athologically obese atients [21 25]. The results of the two most imortant randomized studies, ublished in 2012 by Schauer et al. and Mingrone et al., highlighted the great curative otential of bariatric rocedures RYGB and BPD to be far more effective than traditional medical treatment [10, 11]. Patients enrolled in the studies reresented not only the morbidly obese diabetics, but also individuals with kg/m 2. Although the rate of laboratory remission of treated atients with BMI between 25 kg/m 2 and 55 kg/m 2 was 50 75%, the dynamics of change in HbA 1c and FPG were resented as a cumulative value without resenting the results of atients with kg/m 2 and [10, 11]. In our study, extraction of the kg/m 2 grou (mean BMI value = 29.1 kg/m kg/m 2 in grou) allowed us to exose the differences in dynamics of change of T2DM resolution arameters. Although the dynamics of decrease of HbA 1c and FPG were initially significantly more intense in atients (corresonding with higher weight loss), this difference ceased 1 year after RYGB. Considering the relatively high ercentage of atients who demonstrated raid laboratory glycemic control and imrovement during hosital stay after surgery, it seems that weight loss is not the only factor influencing T2DM remission. Bariatric 528

7 Dynamics of tye 2 diabetes mellitus laboratory remission after Roux-en-Y gastric byass in atients with body mass index lower than 35 kg/m 2 and higher than 35 kg/m 2 in a 3-year observation eriod surgery therefore seems to have metabolic effects indeendent of weight loss induced changes. The ultra-low caloric diet and the effect of incretins were indicated as the most imortant mechanisms of early resolution of hyerglycemia after RYGB unrelated to weight loss [26, 27]. The incretins reresented mainly by glucagon-like etide 1 (GLP-1) are suosed to be resonsible for increase of native insulin secretion, suression of glucagon, imrovement of eriheral insulin suscetibility and slowed down motility of the stomach with concomitant aetite reduction [28]. The shortened alimentary tract and accelerated assage of non-absorbed nutrients after RYGB and BPD induce the activity of these intestinal hormones [27]. Aart from that, the hyothesis of anti-incretins inactivation by duodenum byass should also be considered as one of the mechanisms leading to resolution of T2DM [26 29]. About 80% of all studied cases regardless of BMI demonstrated laboratory comlete resolution of T2DM 1 3 years after surgery. It means that the strict diabetes remission criteria recommended by ADA for HbA 1c 6% and FPG 100 mg% were achieved without anti-diabetic medications [14, 15]. In the remaining grou of atients it was still necessary to continue oral medical treatment or (in only 3 cases) insulin theray, but with significantly reduced doses. Those atients had initially long-lasting T2DM with long-lasting insulin or combined theray u to 15 years. One female with BMI 28 kg/m 2 in consequence of unintended regnancy restored the glucose intolerance and required insulin theray 24 months after RYGB. However, a few months after delivery the glycemia control imroved and HbA 1c was 6.5% with only er oral medications at the last follow-u visit. Another interesting correlation observed in the study was faster and more ronounced remission of T2DM in atients with longer bilioancreatic limb [30]. This will be a subject of a searate study requiring a larger grou of atients. This observation has already been addressed by other researchers, but the ultimate conclusion is not definitive [8, 9]. As found by Fried et al. in a meta-analysis or reviously in a reutable SOS study, we believe that laboratory remission of T2DM after bariatric surgery not only results in normalization of glycemia but also revents comlications induced by diabetes and reduces the mortality [8, 19, 21]. Presented ostoerative comlications and adverse effects were analyzed by the surgical team rogressively. In the last consecutive 60 cases there was no comlication observed at all. In the kg/m 2 grou no serious comlications were noted in the erioerative eriod. That would be consistent with the observation that a high BMI is correlated with a higher rate of major comlications after bariatric rocedures [31, 32]. The ostoerative hyoglycemic eisodes reorted by almost 40% of atients were easily controlled with the hel of simle dietary methods. Only 2 atients (one in each grou) required 1-day hosital admission with intense intravenous glucose sulementation in the early ostoerative eriod. Nevertheless, the frequency of severe hyoglycemia after RYGB was lower than in the same individuals during insulin theray. Additionally, the eisodes qualitatively comared favorably with the revious events and were described by the atients as milder, shorter and easier to control with sweet snacks. In the STAMPEDE trial 56% of atients reorted hyoglycemia eisodes after RYGB, while they were observed in 81% of atients in the grou treated harmacologically [10, 33]. Even though the mechanism of glycemia regulation after RYGB still seems to be unclear, the clinical observations roved its unquestionable effectiveness with accetable safety [9, 16, 22, 34 36]. It seems certainly that surgical treatment of T2DM articularly engaging gastrointestinal byassing methods should not only be the subject of further studies but also be considered as a valid theraeutic otion for mild and morbidly obese diabetic atients. Conclusions The short- and mid-term observation of atients after RYGB revealed significant weight/bmi reduction accomanied with T2DM laboratory remission of different dynamics in the grous of atients with kg/m 2 and. The evaluation of laboratory tye 2 diabetes mellitus measures 3 years after surgery demonstrates high effectiveness of surgical treatment in managing T2DM regardless of BMI. Considering high both social and economic costs of life-long medical treatment of tye 2 diabetes and its comlications, surgical metabolic intervention may become a new theraeutic aroach. References 1. King H, Aubert RE, Herman WH. Global burden of diabetes, : revalence, numerical estimates and rojections. Diabetes Care 1998; 21:

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