The Effective Method of Monitoring Visceral Organ Fatty Infiltration Changes After Bariatric Surgery: Ideal IQ Sequence
PDF
Cite
Share
Request
Original Article
VOLUME: 10 ISSUE: 2
P: 129 - 135
June 2022

The Effective Method of Monitoring Visceral Organ Fatty Infiltration Changes After Bariatric Surgery: Ideal IQ Sequence

Namik Kemal Med J 2022;10(2):129-135
1. Ankara University Faculty of Medicine, Department of Radiology, Ankara, Turkey
2. Beytepe Murat Erdi Eker State Hospital, Clinic of Radiology, Ankara, Turkey
3. Recep Tayyip Erdoğan University Faculty of Medicine, Department of General Surgery, Rize, Turkey
4. Ankara City Hospital, Clinic of Gastrointestinal Surgery, Ankara, Turkey
5. Recep Tayyip Erdoğan University Faculty of Medicine, Department of Radiology, Rize, Turkey
6. Trabzon Kanuni Training and Research Hospital, Clinic of Radiology, Trabzon, Turkey
7. Medical Park Keçiören Hospital, Department of Radiology, Ankara, Turkey
No information available.
No information available
Received Date: 11.03.2021
Accepted Date: 27.12.2021
Publish Date: 22.06.2022
PDF
Cite
Share
Request

ABSTRACT

Conclusion:

Ideal IQ sequence enables quantitative analysis of fatty infiltration of the liver and pancreas and thus may be used as a non-invasive tool to monitor the positive effects of the bariatric surgery on fatty infiltration of these visceral organs in the postoperative period.

Results:

At the end of first month of bariatric surgery, a significant decrease on mean values of LFF and PFF has been observed along with a decrease of LV, LL, BW and BMI (p<0.0001). A moderate positive linear correlation was observed between LFF and PFF, LV, LL (r=0.69, 0.61, 0.49; respectively) while a weak positive linear correlation was noticed between LFF and BMI, BW (r=0.34, 0.21; respectively).

Materials and Methods:

Thirty-nine patients (25 females, 14 males) who underwent bariatric surgery between May 2016 and April 2017 were analyzed retrospectively in this study. Body mass index (BMI) and body weight (BW) values of all patients were noted one week before and one month after bariatric surgery, and meanwhile an unenhanced upper abdominal MR imaging was performed. Liver fat fraction (LFF), pancreas fat fraction (PFF), liver volume (LV) and craniocaudal length of liver (LL) were measured with MR-PDFF and T2 weighted images. Changes in all parameters after the surgery were recorded and the correlation of these changes with the change in LFF was analyzed.

Aim:

The aim of this study is to demonstrate the efficiency of non-invasive imaging method-MR proton density fat fraction (PDFF); ideal IQ sequence- on detecting the effects of bariatric surgery on liver and pancreatic fatty infiltration.

Keywords:
Bariatric surgery, magnetic resonance imaging, non-alcoholic fatty liver, pancreatic disease, proton-density fat fraction

INTRODUCTION

Obesity may result in various health problems such as coronary artery disease, cerebrovascular disease, and metabolic syndrome, in addition to fatty liver and pancreas diseases1. Non-alcoholic fatty liver disease (NAFLD) is present in 70-95% of obese patients. This condition may range from simple steatosis, or from a non-alcoholic steatohepatitis (NASH), to cirrhosis and even to hepatocellular carcinoma2,3.

Pancreas is the other visceral organ in which ectopic fat accumulation secondary to obesity is frequently observed. Non-alcoholic fatty pancreas disease (NAFPD) is pancreatic fatty infiltration due to obesity. Just as NAFLD progresses to non-alcoholic steatohepatitis (NASH) over time, it is possible for NAFPD to progress to non-alcoholic steoatopancreatitis due to the failure of the metabolic condition over time, and as a result, pancreatitis and pancreatic cancer may develop4-8.

Quantitative evaluation of fatty infiltration in the liver and pancreatic parenchyma is of great importance for correct diagnosis and treatment. The gold standard method used for this purpose is liver biopsy9,10. However, this procedure is invasive and has the disadvantage of complications such as hemorrhage and infection, and evaluation of only a limited section of the liver, which may necessitate new diagnostic methods. Recent studies have shown that various magnetic resonance (MR) imaging (MRI) techniques provide accurate information about the amount of fat in the liver parenchyma similar to liver biopsy. These techniques, besides being reported to be non-invasive, have also the advantage to allow the monitoring of fatty liver disease11-15. There is no clear consensus yet on diagnostic methods that can determine the amount of pancreatic fat at an optimum level. However, reviewing the literature, MRI with its non-invasive nature and high sensitivity, is reported to be the most preferred diagnostic imaging method used for this purpose, today. Furthermore, a novel MR-proton density fat fraction (PDFF) method also allows high accuracy quantification of pancreatic fat infiltration16-18.

Fatty liver disease is frequently observed in patients who are candidates for bariatric surgery, and 25% of these patients have NASH and 1-3% have cirrhosis19. NAFLD and secondary parenchymal damage due to fatty infiltration has been shown to be resolved and even completely returned to normal after bariatric surgery in up to 80-92% of the patients20,21.

Although there are accumulating data on the effects of bariatric surgery on NAFLD in the literature, there is still a necessity for further studies regarding the effects of bariatric surgery on pancreatic fatty infiltration. In this context, the aim of this study was to demonstrate the effects of bariatric surgery on the liver and pancreatic parenchyma from the early postoperative period with a non-invasive imaging method, ideal IQ sequence (MR-PDFF).

GİRİŞ

Obezite, karaciğer yağlanması ve pankreas hastalıklarının yanı sıra koroner arter hastalığı, serebrovasküler hastalık ve metabolik sendrom gibi çeşitli sağlık sorunlarına neden olabilir1. Non-alkolik yağlı karaciğer hastalığı (NAFLD), obez hastaların %70-95’inde mevcuttur. Bu durum basit steatozdan veya non-alkolik steatohepatitten (NASH) siroza ve hatta hepatoselüler karsinomaya kadar değişebilir2,3.

Pankreas, obeziteye sekonder ektopik yağ birikiminin sıklıkla görüldüğü diğer viseral organdır. Non-alkolik yağlı pankreas hastalığı (NAFPD), obeziteye bağlı pankreas yağ infiltrasyonudur. NAFLD’nin zamanla NASH’ye ilerlemesi gibi, NAFPD’nin de zamanla metabolik durumun bozulması nedeniyle non-alkolik steoatopankreatite (NASP) ilerlemesi ve bunun sonucunda pankreatit ve pankreas kanseri gelişmesi mümkündür4-8.

Karaciğer ve pankreas parankimindeki yağ infiltrasyonunun kantitatif olarak değerlendirilmesi, doğru tanı ve tedavi için büyük önem taşımaktadır. Bu amaçla kullanılan altın standart yöntem karaciğer biyopsisidir9,10. Ancak bu işlem invazivdir ve kanama ve enfeksiyon gibi komplikasyonlar ve karaciğerin sadece sınırlı bir bölümünün değerlendirilmesi gibi dezavantajlara sahiptir ve bu da yeni tanı yöntemleri gerektirebilir. Son çalışmalar, çeşitli manyetik rezonans (MR) görüntüleme (MRG) tekniklerinin karaciğer biyopsisine benzer şekilde karaciğer parankimindeki yağ miktarı hakkında doğru bilgiler sağladığını göstermiştir. Bu tekniklerin non-invaziv olduğunun bildirilmesinin yanı sıra, yağlı karaciğer hastalığının izlenmesine olanak sağlama avantajı da vardır11-15. Optimum düzeydeki pankreas yağ miktarını belirleyebilecek tanı yöntemleri konusunda henüz net bir fikir birliği yoktur. Ancak literatür incelendiğinde, invaziv olmayan doğası ve yüksek duyarlılığı ile MRG’nin günümüzde bu amaçla kullanılan en çok tercih edilen tanısal görüntüleme yöntemi olduğu bildirilmektedir. Ayrıca, yeni bir MR-proton dansite yağ fraksiyonu (PDFF) yöntemi, pankreas yağ infiltrasyonunun yüksek doğrulukta nicelleştirilmesine de olanak tanımaktadır16-18.

Bariatrik cerrahiye aday hastalarda yağlı karaciğer hastalığı sıklıkla görülür ve bu hastaların %25’inde NASH ve %1-3’ünde siroz vardır19. NAFLD ve yağ infiltrasyonundan kaynaklanan sekonder parankimal hasarın, hastaların %80-92’sinde bariatrik cerrahiden sonra düzeldiği ve hatta tamamen normale döndüğü gösterilmiştir20,21.

Literatürde bariatrik cerrahinin NAFLD üzerine etkilerine dair veriler olmasına rağmen, bariatrik cerrahinin pankreas yağ infiltrasyonu üzerindeki etkilerine ilişkin daha ileri çalışmalara ihtiyaç vardır. Bu bağlamda bu çalışmanın amacı, bariatrik cerrahinin erken postoperatif dönemden itibaren karaciğer ve pankreas parankimi üzerindeki etkilerini non-invaziv bir görüntüleme yöntemi olan ideal IQ sekansı (MR-PDFF) ile ortaya koymaktır.

MATERIALS AND METHODS

This retrospective study was approved by the Recep Tayyip Erdoğan University Institutional Review Board in our institution (decision number: 2019/113, approval date: 09.09.2019) and written informed consent was obtained from all patients.

Patient Selection

A total of 55 patients scheduled for bariatric surgery due to morbid obesity between May 2016 and April 2017 were included in this study. Sixteen patients were excluded from the study for various reasons. The study was conducted with remaining 39 patients who underwent bariatric surgery (35 laparoscopic sleeve gastrectomy, 4 laparoscopic Roux-Y-gastric bypass). The patient flow diagram is shown at Figure 1. All patients were examined with unenhanced upper abdominal MRI a week before and a month after surgical intervention.

Assessment

The patients were evaluated by the multi-disciplinary bariatric team, including two surgeons, endocrinologist, endoscopist, anesthesiologist, psychiatrist and specialized nurses, prior to surgical treatment. All of the bariatric operations were performed by two general surgeons (M.K.Ç. and S.K.). Patients were not administered a diet programme before the surgery. But, after bariatric surgery, all patients were included in the diet program determined by the bariatric team.

Inclusion and Exclusion Criteria

Inclusion criteria were body mass index (BMI) of 40 kg/m2 or BMI ≥35 kg/m2 and having related comorbidities such as diabetes, hypertension, coronary artery disease, and chronic lung diseases. Patients with any contraindications for MR examination (presence of pacemaker or any metallic implant not compatible with MR and claustrophobia) or known diffuse non-NAFLD liver disease (such as chronic hepatitis B or C, Wilson disease and hemochromatosis) were excluded from the study.

Radiological Measurements

All measurements were performed by a single radiologist (Y.M.) with approximately 8 years of experience in abdominal imaging. On the ideal IQ sequences obtained before and after the surgery in the axial plane, the fat fraction values were measured on the fat fraction maps three times and the mean value was recorded using the 3-cm and 1.5-diameter circular region of interest (ROI) from the liver segment 4A and the pancreas body, respectively. Also, liver volume measurements were made by outlining liver boundaries on each slice at ideal IQ sequence and the final volume was calculated automatically. Liver craniocaudal length (LL) was measured in a coronal T2 W images from the hepatic dome to the lower border of the liver passing through the mid-hepatic point. Also, BMI and BW measurements were performed at preoperative and postoperative periods. BMI was calculated as weight/height2.

Magnetic Resonance Imaging

All MRIs were obtained at 3T scanner (GE MR750, GE Healthcare, Waukesha, WI, USA) utilizing a multi-channel torso phased-array coil placed over the liver with all subjects in the supine position. Ideal-IQ sequence was used to determine MRI-PDFF. The Ideal-IQ sequence parameters were as follows: repetition time (TR), 5.8 or 6.7 ms; field of view (FOV), 34 cm; NEX, 0.5; matrix, 128×128; bandwidth, 90.91 or 83.33 kHz; flip angle, 3 degree; a slice thickness, 8.0 mm; and acquisition time, 23 s. At our hospital, Ideal-IQ sequence is included in routine MRI protocols for upper abdominal examinations because fatty liver can be easily and quantitatively evaluated by using this sequence. Liver craniocaudal (LL) measurements were performed on coronal single-shot fast spin-echo T2 WI (coronal SSFSE T2WI: TR, 1200-2000 ms; TE, 30-50 ms; matrix, 256×256; FOV, 40 cm; slice thickness, 6.0 mm; NEX, 2; bandwidth 83.33). The images were processed automatically by using the software (AW server 2.0 software; GE, USA) provided by the manufacturer to create water, fat, in phase (IP), out-of phase, R2 star (R2*), and fat fraction maps.

Statistical Analysis

Data analyses were conducted using SPSS 22.0 Statistical Software (SPSS Inc., Chicago, IL, USA). Descriptive statistics, including the means and ranges, were calculated for the age, body weight, BMI, liver fat-fraction, pancreas fat-fraction, craniocaudal length of liver and liver volume for patients. Normal distributions were verified using the Kolmogorov-Smirnov test. The Paired Sample t-test was used to analyze these parameters. Correlation between liver fat-fraction and body weight, BMI, craniocaudal length of liver, liver volume and pancreas fat-fraction was analyzed using the Pearson’s correlation analysis. A p value less than 0.05 indicated statistical significance.

RESULTS

The present study included 25 female (64.1%) and 14 male (35.9%) patients with a mean age of 41.2±12.5 years.

There was a statistically significant change between preoperative and postoperative values of BW, BMI, LFF, PFF, LL and LV (Table 1).

In the preoperative period, 33 (84.6%) of 39 patients had NAFLD, while 6 patients (15.4%) had no fatty infiltration of liver. Fatty infiltration of liver completely resolved in 26 (66.7%) of 39 patients in the postoperative period, which was statistically significant (p<0.001). In the preoperative period, 16 patients (41%) had NAFPD, and after bariatric surgery, complete resolution of fatty infiltration was observed in 12 (75%) of patients, which was statistically significant (p<0.001). There was a statistically significant decrease in the mean LFF and PFF values in the early postoperative period (p<0.001) (Figure 2). Also, the mean LL and LV values decreased significantly (p<0.001) (Figure 3).

According to the correlation analysis (Table 2), there was a moderate positive linear correlation between LFF and PFF, LL, LV (p<0.001) (Figure 4). A weak positive linear correlation was observed between LFF and BMI (p<0.001), BW (p<0.005).

DISCUSSION

Our study has shown that significant remission is observed in the fatty infiltration of the liver and pancreas in the early period after bariatric surgery, and these positive changes can be detected accurately and non-invasively in a very short time with the ideal IQ sequence.

NAFLD and NAFPD are the diseases that develop due to obesity and, if not treated, can lead to serious health problems in a wide spectrum from infectious processes to malignancy in the liver and pancreas parenchyma2. Today, the increasing frequency of obesity and obesity-related diseases has made the importance of bariatric surgery even more evident. Therefore, demonstrating and monitoring the positive effects of bariatric surgery about the course of NAFLD and NAFPD has also gained great importance. At this point, we aimed to investigate the effects of bariatric surgery on liver and pancreatic fatty infiltration non-invasively by using a novel MRI sequence; ideal IQ (MR-PDFF).

Liver biopsy is the gold standard method used in the determination of the fatty infiltration of the liver and its harmful effects on the liver parenchyma9,22. However, this invasive method has disadvantages such as having preprocedural complications including bleeding, allowing sampling only from a specific liver area, operator dependency, and high cost23. In addition, this method requires performing a liver biopsy before or during surgery, and will expose the patient to these risks several times in the follow-up period. For this reason, non-invasive radiological imaging methods are used instead of liver biopsy to detect fatty infiltration in visceral organs. In the current study, it was aimed to investigate the effects of bariatric surgery both on liver and pancreatic fatty infiltration with MR-PDFF, which is accepted as the most effective and accurate method in the evaluation of fatty infiltration in recent years. Ideal IQ sequence provides volumetric whole-liver and pancreatic coverage in a single breath-hold and generates estimated T2* and triglyceride fat fraction maps in a non-invasive manner. It was found that the MR-PDFF method showed a high correlation with magnetic resonance spectroscopy (MRS) and liver biopsy in the evaluation of fatty liver24-26. Among the advantages of this method, unlike MRS, it does not require special experience for evaluation, and it can be easily measured from any level of the liver parenchyma in a shorter time without the need for postprocessing procedures. As in our study, the amount of fat both in the pancreas and in the liver parenchyma can be quantitatively calculated in seconds with a single sequence.

One of the most important findings in the current study is that fatty infiltration of the liver decreased significantly at the end of first month after bariatric surgery. In 66.7% of the patients participating in our study, after bariatric surgery, LFF values decreased below 6.5% and NAFLD was completely regressed. Unlike other publications in the literature27,28, in this study, we found that LFF values regressed to normal values in more patients in the early postoperative period. It is thought that two main factors play a role in determining such a significant decrease in LFF of the patients after bariatric surgery. The first reason is that the basal LFF (16.8±10.6%) and BMI (46.0±5.2 kg/m2) values of the patients who participated in the study were relatively higher than the basal values in other studies. The second reason is that, unlike other studies, our patients were not given very low calorie diet therapy before surgical treatment. In other studies, it was found that patients both showed weight loss and decreased LFF values after an average of two weeks of low-calorie diet before surgery. This was considered as the reason for less weight loss and decrease in LFF compared to our study. It is thought that not applying a calorie diet to our patients before the surgical treatment causes them to lose weight more quickly and effectively after surgery. However, in order to demonstrate this more clearly, it is considered that future studies will be conducted in which patients who are treated and not treated with diet are evaluated comparatively.

There are limited numbers of publications investigating the effects of bariatric surgery on pancreatic fat infiltration29,30. Similar to our study, in most of these publications, a significant decrease in pancreatic FF values was detected after bariatric surgery. In the study of Covarrubias et al.30, a mean decrease of 0.4% in PDFF values at the 1st month and 5.7% at the end of the 6th month was found after bariatric surgery. In another study by Hui et al.29, it was stated that there was a 1.6% decrease in PDFF rates at the end of 6 months and 4.5% at the end of one year. Although studies have found a decrease in pancreatic FF values at different rates, it is understood that this decrease continues to increase with time. In our study, it was found that 41% of the patients had pre-operative NAFPD, while 75% of the patients had total regression after surgery. Moreover, it was found that there was a 4.4% decrease in pancreatic PDFF rates in the early postoperative period (1 month after surgery). The higher rate of decrease in FF values in our study was evaluated primarily due to the inclusion of more patients.

Today, the time course of postoperative fat fraction changes in visceral organs is not clearly known. However, most studies report that the positive effects of bariatric surgery on fatty infiltration in visceral organs as well as on anthropometric measurements such as BMI and BW continue long term. Accordingly, it was found that LFF reached normal values in almost all patients at the end of the 12th month. On the other hand, it has been reported in most publications that the most significant reduction in liver and pancreatic fat fraction occurs in the early postoperative period (usually at the end of the 1st month)27,30,31. In our study, in parallel with the publications in the literature, a statistically significant decrease was found in the liver and pancreatic fat fraction values of all patients in the first month after surgery. In the study of Luo et al.27, it is understood that the highest decrease in liver PDFF rates occurred in the 1st month after surgery. In addition, while there was no significant change in liver volume in the following imagings, it was determined that the decrease in liver FF values continued, albeit to a lesser extent. Similarly, in another study conducted by Pooler et al.31, it was observed that the highest decrease in liver FF rates was detected in the first month postoperative controls (5.6%). On subsequent follow-up imaging, the decrease in liver FF values (2.8% at the end of the 3rd month and 1.6% at the end of the 6-10th month) continued at decreasing rates. On the other hand, it was understood that the fatty infiltration completely resolved in 66.7% of our patients with NAFLD and in 75% of our patients with NAFPD after the bariatric surgery. This was determined as an evidence that the positive effects of bariatric surgery were most evident in the early period.

Study Limitations

Our study has some limitations. Firstly, although relatively few patients were involved in this study, it is among the studies with highest number of patients on the same topic. Secondly, liver biopsy, which is the gold standard method in the diagnosis of fat infiltration, was not performed in the patients in our study because of its invasiveness and difficulty after treatment. Thirdly, since bariatric surgery is a new treatment method that has been started to be used in our center, the long-term effects of the treatment have not been investigated due to the fact that patients did not adapt adequately to follow-up imaging. Fourthly, sleeve gastrectomy was mainly performed on our patients, and other bariatric surgical methods were applied in a limited number of cases. Therefore, the effects of surgical methods on visceral organ fatty infiltration have not been compared. However, it is planned to conduct studies comparing the effects of different bariatric surgery methods on liver and pancreatic fat in the future. Compared to similar studies in the literature, our study is a rare study that includes a larger number of patients and examines the early changes in both liver and pancreatic fatty infiltration caused by bariatric surgery using a non-invasive method. Lastly, to our knowledge, this is the first study on this topic from Eastern Mediterranean region.

TARTIŞMA

Çalışmamız, bariatrik cerrahi sonrası erken dönemde karaciğer ve pankreasın yağlı infiltrasyonunda belirgin remisyon gözlendiğini ve ideal IQ sekansı ile bu pozitif değişikliklerin çok kısa sürede, doğru ve non-invaziv olarak tespit edilebildiğini göstermiştir.

NAFLD ve NAFPD, obeziteye bağlı olarak gelişen ve tedavi edilmediği takdirde enfeksiyöz süreçlerden karaciğer ve pankreas parankiminde malignitelere kadar geniş bir yelpazede ciddi sağlık sorunlarına yol açabilen hastalıklardır2. Günümüzde obezite ve obeziteye bağlı hastalıkların görülme sıklığının artması obezite cerrahisinin önemini daha da belirgin hale getirmiştir. Bu nedenle bariatrik cerrahinin NAFLD ve NAFPD seyri üzerindeki olumlu etkilerinin gösterilmesi ve izlenmesi de büyük önem kazanmıştır. Bu noktada yeni bir MRG sekansı, ideal IQ (MR-PDFF), kullanarak bariatrik cerrahinin karaciğer ve pankreas yağ infiltrasyonu üzerindeki etkilerini non-invaziv olarak araştırmayı amaçladık.

Karaciğer biyopsisi, karaciğerdeki yağ infiltrasyonunun ve karaciğer parankiması üzerindeki zararlı etkilerinin belirlenmesinde kullanılan altın standart yöntemdir9,22. Ancak bu invaziv yöntemin kanama gibi işlem öncesi komplikasyonlara sahip olması, sadece belirli bir karaciğer bölgesinden örnek alınmasına izin vermesi, operatör bağımlılığı ve yüksek maliyeti gibi dezavantajları vardır23. Ayrıca bu yöntem ameliyattan önce veya ameliyat sırasında karaciğer biyopsisi yapılmasını gerektirir ve hastayı takip döneminde birkaç kez bu risklere maruz bırakır. Bu nedenle viseral organlardaki yağ infiltrasyonunu saptamak için karaciğer biyopsisi yerine non-invaziv radyolojik görüntüleme yöntemleri kullanılmaktadır. Bu çalışmada, son yıllarda yağ infiltrasyonunun değerlendirilmesinde en etkili ve doğru yöntem olarak kabul edilen MR-PDFF ile bariatrik cerrahinin hem karaciğer hem de pankreas yağ infiltrasyonu üzerine etkilerinin araştırılması amaçlanmıştır. İdeal IQ sekansı, tek bir nefes tutmada hacimsel tüm karaciğer ve pankreas kapsamı sağlar ve non-invaziv bir şekilde tahmini T2* ve trigliserit yağ fraksiyon haritaları oluşturur. MR-PDFF yönteminin, karaciğer yağlanmasının değerlendirilmesinde manyetik rezonans spektroskopisi (MRS) ve karaciğer biyopsisi ile yüksek korelasyon gösterdiği bulunmuştur24-26. Bu yöntemin avantajları arasında, MRS’den farklı olarak, değerlendirme için özel bir deneyim gerektirmemesi ve işlem sonrası herhangi bir prosedür gerektirmeden daha kısa sürede karaciğer parankiminin herhangi bir seviyesinden kolaylıkla ölçülebilmesi bulunmaktadır. Çalışmamızda olduğu gibi hem pankreastaki hem de karaciğer parankimindeki yağ miktarı tek bir sekans ile saniyeler içinde kantitatif olarak hesaplanabilmektedir.

Mevcut çalışmadaki en önemli bulgulardan biri, bariatrik cerrahiden sonraki ilk ayın sonunda karaciğerdeki yağ infiltrasyonunun önemli ölçüde azalmasıdır. Çalışmamıza katılan hastaların %66,7’sinde bariatrik cerrahi sonrası KYF değerleri %6,5’in altına düşmüş ve NAFLD tamamen gerilemiştir. Literatürdeki diğer yayınlardan farklı olarak27,28 bu çalışmada erken postoperatif dönemde daha fazla hastada KYF değerlerinin normal değerlere gerilediğini bulduk. Bariatrik cerrahi sonrası hastaların KYF’lerinde bu kadar anlamlı bir düşüşün belirlenmesinde iki ana faktörün rol oynadığı düşünülmektedir. Birinci neden, çalışmaya katılan hastaların bazal KYF (%16,8±10,6) ve VKİ (46,0±5,2 kg/m2) değerlerinin diğer çalışmalardaki bazal değerlerden nispeten yüksek olmasıdır. İkinci sebep ise diğer çalışmalardan farklı olarak hastalarımıza cerrahi tedavi öncesi çok düşük kalorili diyet tedavisi verilmemiş olmasıdır. Diğer çalışmalarda, ameliyattan önce ortalama iki haftalık düşük kalorili diyet sonrasında hastalarda hem kilo kaybı hem de KYF değerlerinde azalma olduğu bulunmuştur. Bu durum çalışmamızla kıyaslandığında daha az kilo kaybı ve KYF’de düşüş nedeni olarak değerlendirildi. Hastalarımıza cerrahi tedavi öncesi kalorili diyet uygulanmamasının ameliyat sonrasında daha hızlı ve etkili bir şekilde kilo vermelerine neden olduğu düşünülmektedir. Ancak bunu daha net ortaya koyabilmek için, diyetle tedavi edilen ve edilmeyen hastaların karşılaştırmalı olarak değerlendirildiği çalışmalara ihtiyaç duyulmaktadır.

Bariatrik cerrahinin pankreas yağ infiltrasyonu üzerindeki etkilerini araştıran sınırlı sayıda yayın vardır29,30. Bu yayınların çoğunda bizim çalışmamıza benzer şekilde bariatrik cerrahi sonrası pankreas YF değerlerinde anlamlı azalma saptandı. Covarrubias ve ark.30 tarafından yapılan bir çalışmada, bariatrik cerrahi sonrası PDFF değerlerinde 1. ayda ortalama %0,4 ve 6. ayın sonunda %5,7’lik bir azalma saptanmıştır. Hui ve ark.29 tarafından yapılan bir başka çalışmada ise PDFF oranlarında 6 ay sonunda %1,6, bir yıl sonunda ise %4,5 oranında azalma olduğu belirtilmiştir. Yapılan çalışmalarda pankreas YF değerlerinde farklı oranlarda düşüş saptansa da bu düşüşün zamanla artarak devam ettiği anlaşılmaktadır. Çalışmamızda hastaların %41’inde preoperatif NAFPD saptanırken, ameliyat sonrası hastaların %75’inde tam gerileme olduğu saptandı. Ayrıca erken postoperatif dönemde (ameliyattan 1 ay sonra) pankreas PDFF oranlarında %4,4’lük bir azalma olduğu tespit edildi. Çalışmamızda YF değerlerindeki düşme oranının daha yüksek olması, öncelikle daha fazla hastanın dahil edilmesi nedeniyle değerlendirildi.

Günümüzde viseral organlardaki postoperatif yağ fraksiyonu değişikliklerinin zaman süreci net olarak bilinmemektedir. Bununla birlikte, çoğu çalışma, bariatrik cerrahinin viseral organlardaki yağ infiltrasyonu ve VKİ ve VA gibi antropometrik ölçümler üzerindeki olumlu etkilerinin uzun vadede devam ettiğini bildirmektedir. Buna göre 12. ayın sonunda hemen hemen tüm hastalarda KYF’nin normal değerlere ulaştığı saptandı. Öte yandan, çoğu yayında karaciğer ve PYF’deki en belirgin azalmanın ameliyat sonrası erken dönemde (genellikle 1. ayın sonunda) olduğu bildirilmiştir27,30,31. Çalışmamızda literatürdeki yayınlara paralel olarak tüm hastaların karaciğer ve PYF değerlerinde ameliyat sonrası ilk bir ayda istatistiksel olarak anlamlı düşüş saptandı. Luo ve ark.’nın27 çalışmasında, karaciğer PDFF oranlarındaki en yüksek düşüşün ameliyattan sonraki 1. ayda meydana geldiği anlaşılmaktadır. Ayrıca takip eden görüntülemelerde KV’de anlamlı bir değişiklik olmazken, karaciğer YF değerlerindeki düşüşün daha az da olsa devam ettiği belirlendi. Benzer şekilde Pooler ve ark.31 tarafından yapılan bir başka çalışmada da, karaciğer YF oranlarındaki en yüksek düşüşün ameliyat sonrası ilk ay kontrollerinde (%5,6) saptandığı görülmüştür. Takip eden takip görüntülemelerinde karaciğer YF değerlerindeki düşüş (3. ay sonunda %2,8 ve 6-10. ay sonunda %1,6) azalan oranlarda devam etti. Öte yandan bariatrik cerrahi sonrası NAFLD’li hastalarımızın %66,7’sinde, NAFPD’li hastalarımızın ise %75’inde yağ infiltrasyonunun tamamen düzeldiği anlaşıldı. Bu da bariatrik cerrahinin olumlu etkilerinin erken dönemde belirgin olduğunun bir kanıtı olarak görüldü.

Çalışmanın Kısıtlılıkları

Çalışmamızın bazı sınırlamaları vardır. İlk olarak, bu çalışmaya nispeten az sayıda hasta dahil edilmiş olmasına rağmen, en fazla hasta sayısına sahip aynı konuda yapılmış çalışmalar arasındadır. İkinci olarak, yağ infiltrasyonu tanısında altın standart yöntem olan karaciğer biyopsisi invaziv olması ve tedavi sonrası zorluğu nedeniyle çalışmamızdaki hastalara yapılmadı. Üçüncüsü, obezite cerrahisi merkezimizde kullanılmaya başlanan yeni bir tedavi yöntemi olduğundan hastaların takip görüntülemeye yeterince uyum sağlayamaması nedeniyle tedavinin uzun dönem etkileri araştırılmamıştır. Dördüncüsü, hastalarımıza ağırlıklı olarak tüp mide ameliyatı yapıldı ve sınırlı sayıda vakada diğer bariatrik cerrahi yöntemler uygulandı. Bu nedenle cerrahi yöntemlerin viseral organ yağ infiltrasyonu üzerindeki etkileri karşılaştırılmamıştır. Ancak gelecekte farklı bariatrik cerrahi yöntemlerinin karaciğer ve pankreas yağları üzerindeki etkilerini karşılaştıran çalışmaların yapılması planlanmaktadır. Literatürdeki benzer çalışmalarla karşılaştırıldığında çalışmamız, bariatrik cerrahinin neden olduğu hem karaciğer hem de pankreas yağ infiltrasyonundaki erken değişiklikleri non-invaziv bir yöntemle inceleyen ve daha fazla sayıda hastayı içeren nadir bir çalışmadır. Son olarak, bilgilerimize göre bu çalışma, Doğu Akdeniz bölgesinden bu konuda yapılan ilk çalışmadır.

CONCLUSION

Ideal IQ sequence is a non-invasive effective method that allows the monitorization of the positive effects of bariatric surgery on liver and pancreatic fatty infiltration.

Ethics

Ethics Committee Approval: This retrospective study was approved by the Recep Tayyip Erdoğan University Institutional Review Board in our institution (decision number: 2019/113, approval date: 09.09.2019).
Informed Consent: Retrospective study.
Peer-review: Externally peer-reviewed.

Authorship Contributions

Surgical and Medical Practices: S.K., M.K.Ç., Concept: Y.M., Design: Y.M., Data Collection or Processing: Y.M., N.O.M., F.T., O.Ö., Analysis or Interpretation: A.K., Literature Search: Y.M., N.O.M., O.Ö., Writing: Y.M., N.O.M., O.Ö.
Conflict of Interest: No conflict of interest was declared by the authors.
Financial Disclosure: The authors declared that this study received no financial support.

References

1
McFarlane SI, Banerji M, Sowers JR. Insulin resistance and cardiovascular disease. J Clin Endocrinol Metab. 2001;86:713-8.
2
Vernon G, Baranova A, Younossi ZM. Systematic review: the epidemiology and natural history of non-alcoholic fatty liver disease and non-alcoholic steatohepatitis in adults. Aliment Pharmacol Ther. 2011;34:274-85.
3
Glen J, Floros L, Day C, Pryke R; Guideline Development Group. Non-alcoholic fatty liver disease (NAFLD): summary of NICE guidance. BMJ. 2016;354:i4428.
4
Smits MM, van Geenen EJ. The clinical significance of pancreatic steatosis. Nat Rev Gastroenterol Hepatol. 2011;8:169-77.
5
Mathur A, Marine M, Lu D, Swartz-Basile DA, Saxena R, Zyromski NJ, et al. Nonalcoholic fatty pancreas disease. HPB (Oxford). 2007;9:312-8.
6
Ogilvie RF. The islands of langerhans in 19 cases of obesity. Journal Pathology and Bacteriology. 1933;37:473-81.
7
Martínez J, Johnson CD, Sánchez-Payá J, de Madaria E, Robles-Díaz G, Pérez-Mateo M. Obesity is a definitive risk factor of severity and mortality in acute pancreatitis: an updated meta-analysis. Pancreatology. 2006;6:206-9.
8
Lee JS, Kim SH, Jun DW, Han JH, Jang EC, Park JY, et al. Clinical implications of fatty pancreas: correlations between fatty pancreas and metabolic syndrome. World J Gastroenterol. 2009;15:1869-75.
9
Nalbantoglu IL, Brunt EM. Role of liver biopsy in nonalcoholic fatty liver disease. World J Gastroenterol. 2014;20:9026-37.
10
Ratziu V, Charlotte F, Heurtier A, Gombert S, Giral P, Bruckert E, et al. Sampling variability of liver biopsy in nonalcoholic fatty liver disease. Gastroenterology. 2005;128:1898-906.
11
Goceri E, Shah ZK, Layman R, Jiang X, Gurcan MN. Quantification of liver fat: A comprehensive review. Comput Biol Med. 2016;71:174-89.
12
Idilman IS, Keskin O, Celik A, Savas B, Elhan AH, Idilman R, et al. A comparison of liver fat content as determined by magnetic resonance imaging-proton density fat fraction and MRS versus liver histology in non-alcoholic fatty liver disease. Acta Radiol. 2016;57:271-8.
13
van Werven JR, Marsman HA, Nederveen AJ, Smits NJ, ten Kate FJ, van Gulik TM, et al. Assessment of hepatic steatosis in patients undergoing liver resection: comparison of US, CT, T1-weighted dual-echo MR imaging, and point-resolved 1H MR spectroscopy. Radiology. 2010;256:159-68.
14
Kramer H, Pickhardt PJ, Kliewer MA, Hernando D, Chen GH, Zagzebski JA, et al. Accuracy of Liver Fat Quantification With Advanced CT, MRI, and Ultrasound Techniques: Prospective Comparison With MR Spectroscopy. AJR Am J Roentgenol. 2017;208:92-100.
15
Guiu B, Petit JM, Loffroy R, Ben Salem D, Aho S, Masson D, et al. Quantification of liver fat content: comparison of triple-echo chemical shift gradient-echo imaging and in vivo proton MR spectroscopy. Radiology. 2009;250:95-102.
16
Vieira J, Amorim J, Martí-Bonmatí L, Alberich-Bayarri Á, França M. Quantifying steatosis in the liver and pancreas with MRI in patient with chronic liver disease. Radiologia (Engl Ed). 2020;62:222-8.
17
Yao WJ, Guo Z, Wang L, Li K, Saba L, Guglielmi G, et al. Pancreas fat quantification with quantitative CT: an MRI correlation analysis. Clin Radiol. 2020;75:397.e1-397.e6.
18
Idilman IS, Tuzun A, Savas B, Elhan AH, Celik A, Idilman R, et al. Quantification of liver, pancreas, kidney, and vertebral body MRI-PDFF in non-alcoholic fatty liver disease. Abdom Imaging. 2015;40:1512-9.
19
Pillai AA, Rinella ME. Non-alcoholic fatty liver disease: is bariatric surgery the answer? Clin Liver Dis. 2009;13:689-710.
20
Mummadi RR, Kasturi KS, Chennareddygari S, Sood GK. Effect of bariatric surgery on nonalcoholic fatty liver disease: systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2008;6:1396-402.
21
Lassailly G, Caiazzo R, Buob D, Pigeyre M, Verkindt H, Labreuche J, et al. Bariatric Surgery Reduces Features of Nonalcoholic Steatohepatitis in Morbidly Obese Patients. Gastroenterology. 2015;149:379-88; quiz e15-6.
22
Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F. Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol. 2009;51:433-45.
23
Ble M, Procopet B, Miquel R, Hernandez-Gea V, García-Pagán JC. Transjugular liver biopsy. Clin Liver Dis. 2014;18:767-78.
24
Hu HH, Kim HW, Nayak KS, Goran MI. Comparison of fat-water MRI and single-voxel MRS in the assessment of hepatic and pancreatic fat fractions in humans. Obesity (Silver Spring). 2010;18:841-7.
25
Idilman IS, Aniktar H, Idilman R, Kabacam G, Savas B, Elhan A, et al. Hepatic steatosis: quantification by proton density fat fraction with MR imaging versus liver biopsy. Radiology. 2013;267:767-75.
26
Tang A, Tan J, Sun M, Hamilton G, Bydder M, Wolfson T, et al. Nonalcoholic fatty liver disease: MR imaging of liver proton density fat fraction to assess hepatic steatosis. Radiology. 2013;267:422-31.
27
Luo RB, Suzuki T, Hooker JC, Covarrubias Y, Schlein A, Liu S, et al. How bariatric surgery affects liver volume and fat density in NAFLD patients. Surg Endosc. 2018;32:1675-82.
28
Hedderich DM, Hasenberg T, Haneder S, Schoenberg SO, Kücükoglu Ö, Canbay A, et al. Effects of Bariatric Surgery on Non-alcoholic Fatty Liver Disease: Magnetic Resonance Imaging Is an Effective, Non-invasive Method to Evaluate Changes in the Liver Fat Fraction. Obes Surg. 2017;27:1755-62.
29
Hui SCN, Wong SKH, Ai Q, Yeung DKW, Ng EKW, Chu WCW. Observed changes in brown, white, hepatic and pancreatic fat after bariatric surgery: Evaluation with MRI. Eur Radiol. 2019;29:849-56.
30
Covarrubias Y, Fowler KJ, Mamidipalli A, Hamilton G, Wolfson T, Leinhard OD, et al. Pilot study on longitudinal change in pancreatic proton density fat fraction during a weight-loss surgery program in adults with obesity. J Magn Reson Imaging. 2019;50:1092-102.
31
Pooler BD, Wiens CN, McMillan A, Artz NS, Schlein A, Covarrubias Y, et al. Monitoring Fatty Liver Disease with MRI Following Bariatric Surgery: A Prospective, Dual-Center Study. Radiology. 2019;290:682-90.