Introduction

Bariatric surgery remains a suitable intervention for patients with morbid obesity [1]. It improves obesity-related complications by reducing excessive body weight, recovering body functions, and reducing the mortality rate [2]. Among various bariatric surgical procedures, laparoscopic sleeve gastrectomy (LSG) has become the most commonly performed bariatric procedure recently [3]. LSG can facilitate percent of excess weight loss (%EWL) by more than 72% 12 months after surgery and significantly reduce the waist circumference [4]. However, the postoperative daily energy intake after 3 months is only approximately 700 kcal, which is increased to 918 kcal 12 months after surgery [4]. Such a low energy intake indicates that postoperative patients need a more detailed dietary plan and dietary supplements to receive adequate nutrition.

A successful bariatric surgery is defined as 50–70% EWL and 20–30% loss of initial weight while achieving BMI <35 kg/m2. On the contrary, failure in terms of weight outcomes is described as <50% EWL, <20% loss of initial weight, and BMI ≥35 kg/m2. About 20–30% of patients with bariatric surgery do not achieve “successful” weight outcomes [5,6,7]. On the other hand, weight stability has been defined as ±5 kg for both surgical and nonsurgical patients. Because bariatric surgery may lead to gradual weight regain several years after surgery, regain of 20–25% of the lost weight after bariatric surgery can occur over a period of 10 years [7]. Therefore, a weight increase of >5 kg is a warning for further intervention as soon as possible [8, 9]. Although LSG is the leading bariatric procedure now, long-term data about weight regain is lack.

It was known that severely obese patients are more likely to experience preoperative micronutrient deficiency than healthy individuals because of unbalanced diet [10,11,12]. Yet, there is a strong likelihood of postoperative nutritional imbalance due to restricted diet, malabsorption, or incorrect nutritional knowledge. LSG is a restrictive procedure that limits food intake. The resection of gastric fundus reduces the intrinsic factor and gastric acid. The rapid entrance of food into the small intestine may also reduce the bioavailability and digestion of nutrients [13]. In contrast to malabsorptive procedures, restrictive procedures are less likely to cause deficiencies of calcium and iron. Improved food tolerance or widening of the gastric tube may contribute to the gradual increase of postoperative food intake. However, this is still worth examining even after several years of research. Currently, there is a lack of long-term follow-up reports on post-LSG nutrient status, dietary behavior, and weight maintenance [4, 10, 14,15,16]. The aim of this study was to observe the long-term weight change after LSG and to explore the correlation between the post-LSG diet intake and weight regain. This study hypothesized that some patients may experience weight regain 5 years after LSG and that the regain might be correlated with the increased calorie intake.

Materials and Methods

Patient Selection

This study investigated patients with morbid obesity who had received LSG procedures in the Bariatric Surgery Center of Min-Sheng General Hospital in Taoyuan City, Taiwan, prior to May 1, 2009. The participants agreed to take a dietary questionnaire and signed a letter of consent. The study period was from June 2014 to August 2015. Forty patients who underwent LSG approximately 5 years ago were follow-up using complete clinical data and a food frequency questionnaire. The collected data were entered into a software package for the calculation of energy and nutrient intake. A total of 120 eligible patients who had received LSG for ≥5 years were screened through their medical records, and 60 of them agreed to be interviewed. Of these respondents, 40 completed their questionnaires and 34 (85%) completed the routine blood test. Among the 40 respondents, 30 were women (75%) and 10 were men (25%), with a mean age of 33.5 ± 9.7 years.

In addition, this study retrospectively reviewed the annual medical records of the respondents’ follow-up visits, including their anthropometric measurements and blood test results. The anthropometric, blood pressure, and biochemical tests were scheduled for the documentation preoperatively; 1, 3, 6, and 12 months postoperatively; and annually after year 1. Measurement items included height, weight, blood pressure, waist and hip circumferences, and BMI; blood test items included complete blood count, albumin, hemoglobin (Hb), cholesterol, triglyceride, uric acid, fasting glucose, glycated hemoglobin (HbA1c), calcium, and intact parathyroid hormone (iPTH). Weight change was studied by body weight, BMI, percent of total weight loss (%TWL), and percent of excess weight loss (%EWL) which was calculated as ideal body weight of BMI 25. Weight regain was defined by weight increase from nadir more than 25% of their lost weight. This study was approved by the Institutional Review Board of Min-Sheng General Hospital (MSIRB2014010) and was registered on ClinicalTrials.gov (NCT: 02193529).

Research Instrument

The objective of this study was to calculate the respondents’ calorie intake. The Dietary Questionnaire for Epidemiological Studies Version 2 (DQES v2), published by Cancer Council Australia, was employed in this study and a previous large-scale study [17]. Items in DQES v2 include a great variety of food, clearly explained for easy response. In addition, these items provide the respondents with pictures of serving portions for visual assistance. DQES v2 is a convenient instrument for fast calculation of food intake in grams and nutritional content. However, food preferences vary in Eastern and Western cultures. Because there is currently no comparable research instrument in Taiwan, to avoid skewed results, this study supplemented DQES v2 with the 24-h recall method to collect the respondents’ daily diet and calculate their calorie and macronutrient (i.e., carbohydrate, protein, and fat) intake. The food frequency questionnaire examined the types and frequency of food that the respondent consumed in the past 12 months and comprised 74 types of food and 10 levels of frequency for response. The frequencies ranged from “never eat” to “≥3 times a day,” with pictures of various serving portions presented for visual reference. The 74 types of food were classified into (1) grains, desserts, and snacks; (2) dairy products, meat, and fish; (3) fruits; and (4) vegetables. Six types of alcoholic beverages were also included in the 74 types of food.

Surgical Techniques

All respondents in this study had received LSG procedures performed by the same physician in the same institution [18]. A 36-French gastric tube was inserted trans-orally to the gastric fundus along the lesser curvature. Subsequently, the gastric fundus was vertically dissected in the 2–4 cm section from the pylorus to the angle of His while an endoscopic stapler was simultaneously fired from the bottom up for anastomosis. Finally, the dissected gastric fundus was removed from the body from the umbilical wound, and the procedure was completed after the anastomotic leak test was conducted.

Statistical Analysis

All collected data were stored in a computer for statistical analysis using IBM SPSS 19. The respondents’ anthropometric measurements, blood test results, and calorie and nutrient intakes were compared and presented as mean values and standard deviations. The calorie and nutrient intake was evaluated using the DQESv2. The respondents were grouped by whether they had experienced weight regain. The independent t test, paired t test, chi-squared test, and McNemar test were conducted with the statistical significance set at P < .05. A simple linear regression was used to analyze the correlation between weight outcomes and several variables, and a bivariate regression was used to predict the correlation of weight outcomes in various years.

Results

Weight Loss

The respondents’ mean body weight was reduced from a preoperative 102.3 ± 22.4 kg to 72.9 ± 12.2 kg 5 years after operation, with an average weight loss of 29.6 kg (i.e., %TWL of 27.5%) and a mean %EWL of 95.5%. The mean preoperative and postoperative BMIs were 37.9 ± 6.6 and 27.3 ± 3.9 kg/m2, respectively, with a mean BMI loss (BMIL) of approximately 10.6 kg/m2. The respondents’ weight loss varied according to the postoperative time point. The most substantial postoperative weight loss occurred in year 1, followed by a slight weight regain in year 3 and a significant regain of 1.3 kg (4.4% of TWL) at year 5 (P = .02). The respondents had significantly improved their body weights, BMIs, and blood pressure postoperatively, as shown in Table 1. In analysis, the young age group (≤30 years old) had more favorable weight outcomes than the old age group did (TWL 32.6 versus 24%, P = .02). Women had higher %EWL than men did postoperatively. In addition, the postoperative weight outcome in year 1 could predict that of year 5 (P = .00, R 2 = 0.86).

Table 1 Anthropometric and blood results after sleeve gastrectomy 5 years
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Laboratory Changes

The blood test results revealed that the respondents’ glucose, HbA1c, uric acid, and triglyceride contents all significantly decreased postoperatively in years 1, 3, and 5 (Table 1). In addition, Hb also significantly decreased postoperative from year 1 to year 5 (from 13.7 to 11.7 g/dl), whereas iPTH significantly increased from 53.5 to 70.9 pg/ml in year 5. Incidence of iron deficiency anemia increased from 7.5% at pre-operation to 41.2% after LSG. Incidence of secondary hyperparathyroidism increased from 17.5 to 60.7%. However, no significant changes were observed in the respondents’ albumin, calcium, and cholesterol levels.

Nutrient Intake and Weight Loss

Table 2 shows the respondents’ average calorie intake in year 5 was 1230 kcal/day or approximately 1221 kcal/day for male respondents and 1233 kcal/day for female respondents. Respondents’ mean protein (70 g/day), carbohydrate (126 g/day), and fat intakes (50.1 g/day), accounted respectively for 22.5, 41.4, and 36.1% of total energy intake. The fiber and cholesterol intakes were 11.7 and 316.4 g/day, respectively. Daily intakes had also been recorded for calcium (536.2 mg/day), iron (7.5 mg/day), sodium (1444.3 mg/day), potassium (1701.1 mg/day), zinc (8.2 mg/day), and magnesium (177.2 mg/day). The total energy and nutrient intake of LSG patients at 5 years are lower than the recommended dose from Taiwan dietary reference intake and ASMBS [1]. In the present study, we collected the preoperative dietary data of nine patients with morbid obesity before surgery as reference. Their mean energy intake was 2418 kcal/day, similar to the preoperative energy intake of patients in previous reports (2503, 2197, and 1981 kcal/day) [19,20,21]. Therefore, we may conclude that LSG reduced the postoperative energy intake in year 5 by approximately 50%.

Table 2 Nutrients intake after sleeve gastrectomy for 5 years and compared to Taiwan's dietary reference intake 2011 and ASMBS 2013
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Figure 1 demonstrates that the postoperative weight outcome in year 5 was modestly correlated to energy intake (r = 0.313, P = .052). The weight outcome was not significantly correlated with the total fat, protein, or carbohydrate intakes (P = .173).

Fig. 1
figure 1

Scatter diagram of energy intake and weight loss in year 5 after LSG

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Weight Regain and Dietary Intake

This study defined weight regain as an increase of more than 25% body weight from the nadir weight to the body weight in year 5. According to this definition, 28 respondents in this study did not experience weight regain (75%), whereas 9 of them did (22.5%); the data for the other 3 respondents (7.5%) were insufficient for comparison. Of all the patients, the mean weight regain rate was 14%, but the mean body weight increase for those who experienced weight regain was 37.8%, compared to 6.4% for those respondents who did not experience weight regain. Table 3 shows the macronutrient intake data grouped by whether the respondents experienced weight regain. This table demonstrates that the non-regain group had greater energy intake (1327 ± 572 kcal/day) than the regain group did (1059 ± 352 kcal/day), although the difference was statistically not significant (P = .2). The non-regain group had a greater intake of fat (55 g/day), protein (77.5 g/day), and zinc than the regain group. Neither age nor gender was significantly correlated with respondents’ energy intake.

Table 3 Macronutrients intake data from FFQ after sleeve gastrectomy for 5 years
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Discussions

This study confirmed LSG is an effective and durable weight reduction surgery. In this study, primary LSG resulted in an average of 26.5% weight loss and BMI loss of 10.6 kg/m2 at 1 year and stabilized up to 5 years. However, 20% of the studied patients had weight regain 5 years after LSG which corroborated with another study that weight regain of >10 kg was observed in 19.2% of patients 5 years after the operation [22]. In the current study, postoperative weight loss at year 1 is most apparent. Subsequently, the respondent experienced weight regain as their body gradually adapted to the postoperative changes. The weight-increasing trend after LSG in the current study was consistent with the findings in previous reports [16, 23].

The most important finding of this study is that there was a 50% reduction in calorie intake, which was sustain for 5 years after LSG. In this study, the energy intake according to the dietary questionnaire was 1230 kcal/day 5 years after LSG, and the 24-h recall method reported a daily energy intake of approximately 1083 kcal/day. These findings were extremely similar to previous studies with 918, 1170, and 1203 kcal/day [4, 19, 20]. Therefore, the postoperative energy intake patterns were similar in the East and West. In terms of macronutrient intake, the current study revealed a daily protein intake of 70 ± 33.4 g/day, approximately 22.5% of total energy intake, which is lower than the 35% suggested by the American Society of Metabolic and Bariatric Surgery (ASMBS) in 2013 for health care of patients receiving bariatric surgery [1]. Studies have also suggested that higher protein intake (80–90 g/day) is associated with reduce loss of lean body mass [1]. The carbohydrate intake of 126 ± 59 g/day found in the current study was approximately 41.4% of total energy intake and slightly lower than the ASMBS recommendation (45% of low glycemic index). The daily fat intake of 50.1 ± 24.7 g/day was 36.1% of total energy intake, slightly higher than both the dietary reference intake (DRI) in Taiwan (30%) and the ASMBS recommendation (20%). The daily fiber intake of the respondents in this study was merely 11.7 g/day, substantially lower than the 14 g/1000 kcal consumed [24]. Fiber can improve satiety and reduce the cholesterol level. In addition, fruit and vegetable intake provides phytochemicals, vitamins, and folate.

The current study reveals that the patients with morbid obesity experienced a significant loss of Hb in year 5 after receiving LSG, from 13.7 g/dl preoperatively to 11.8 g/dl in year 5 (P = .00), as shown in Table 1. Five respondents (12.5%) reported preoperative anemia (<13 g/dl of Hb for male and <12 g/dl for female) and 16 respondents (40%) reported postoperative anemia in year 5 (13 female and 3 male). The postoperative iron intake of the respondents was 7.5 mg/day. The respondents reported a folate intake of 110.1 μg/day, which was only a quarter of the recommended intake by DRI (400 μg/day). Other factors affecting anemia include deficiency of protein, copper, selenium, zinc, and particularly vitamin B12. In this study, the reported zinc intake was 8.2 mg/day, substantially lower than the 12–15 mg/day recommended by DRI. The younger group had greater sodium and zinc intake than the older group, and the non-regain group had a greater zinc intake than the regain group. Because this study did not collect the vitamin B12 intake, the appropriate information could not be provided for comparison. Calcium, iron, potassium, and magnesium intake was not significantly correlated to the respondent’s age, gender, or weight.

The respondents in this study reported a mean calcium intake of 536.2 mg/day. In 2017, ASMBS [12] revised their recommendation of calcium and vitamin D to 1200–1500 mg/day (Grade D, Best Evidence Level 4) and 3000 international units/day, respectively. ASMBS also recommends the additional intake of dairy products (or calcium supplements) to increase calcium level, and weight-bearing exercise and sun exposure to improve calcium utilization. Unlike gastric bypass surgery, LSG does not directly affect calcium uptake, but the respondents in this study reported increased incidences of secondary hyperparathyroidism (i.e., iPTH >69 pg/ml) from 17.5% preoperatively to 60.7% postoperatively, and calcium deficiency appears to be the main reason.

Another important finding of this study is that weight regain after LSG was not related to higher calorie intake. Actually, this study suggested that a better intake with more balance in macronutrient components may prevent weight regain after LSG. In this study, the fat and protein intake of the non-regain group was greater than that of the regain group, and the total energy intake of the non-regain group was also slightly greater than that of the regain group. Therefore, the outcome of weight regain is not affected by a single factor. For patients with bariatric surgery, other factors may include inadequate physical activity, inactive lifestyle, poor eating habits, improper food choices, lack of nutritional knowledge, and bulimia. Surgically, the expanded stomach may contribute to the problem of expanded intake capacity and hamper the restrictive effect on diet. Cambi et al. also stated that the patients who experienced weight regain did not revisit the multidisciplinary team for follow-up counseling 12 months after receiving bariatric surgery, which highlights the importance of routine physician visits [25]. The stomach forms a narrow vertical tube with a capacity of 100–150 cm3 after sleeve gastrectomy is performed. Therefore, satiety can be achieved with a small portion of food; the reduced transit time in the stomach decreases the appetitive hormone ghrelin and increases the peptide tyrosine, a satiety hormone, resulting in early satiety. Yet the limited digestion and poor bioavailability leads to inadequate nutrients, and common complications include hypoglycemia, loss of lean body mass, weight regain, and vitamin and mineral deficiencies. Vitamin D deficiency ranges from 23 to 83%, whereas deficiencies in vitamin B12 and iron range from 2 to 18% [26].

Our study had some limitations. First, the case number in this study was relatively small and precluded us from a more complicated statistical analysis. When applying this score in lower BMI patients, we need to be very careful because the small number in the particular group.

Conclusion

In summary, this study demonstrated that LSG led to excellent weight outcomes that can be maintained 5 years later. However, postoperative issues still require the attention of patients and healthcare professionals, such as long-term weight-loss maintenance and the trend of weight regain, anemia prevention, and the need for calcium supplementation. Physicians should evaluate patients’ preoperative nutritional status and eating habits, and patients should consider their own needs, food preferences, physical activity, and daily routines before considering bariatric intervention. Preoperative preventative nutritional supplements, and being proactive about nutritional treatment and routine follow-ups postoperatively, further ensure the success of the intervention and prevent the incidence of nutritional deficiencies.