Bariatric Surgery Outcomes in HIV-Infected Subjects: A Case Series

Abstract

Obesity is now a common problem among HIV-infected patients receiving antiretroviral therapy (ART). Gastric bypass surgery may be an option for some patients who have failed diet and therapeutic lifestyle changes, changes in ART or other treatment modalities for HIV/ART-related lipohypertrophy and obesity. However, few data are available regarding HIV-related outcomes after such surgery and its impact on ART tolerability. We present here a case series of seven subjects with HIV infection who underwent bariatric surgery. Viral suppression was maintained in five of the six subjects who were receiving ART prior to surgery, including three subjects who experienced surgical complications. The median (range) decrease in body mass index (BMI) postoperatively was 10 kg/m² (6–28 kg/m²). Improvements were also seen in serum lipid fractions with median (range) changes in total cholesterol of −19 mg/dL (−61 to +3 mg/dL) and triglycerides of −185 mg/dL (−739 to +35 mg/dL). Four of the subjects had a reduction in their metabolic medication prescriptions postoperatively. Three of the subjects experienced postsurgical complications. Based on our experience, bariatric surgery may provide an effective treatment modality for obesity and its related comorbidities in the HIV-infected population while not sacrificing virologic suppression. Larger studies are needed to verify these results, especially in regards to surgical complications.

Introduction

A s the prognosis for HIV infection has improved with antiretroviral therapy (ART), AIDS-related mortality has fallen significantly. However, significant comorbidities, including cardiovascular disease, have become common in this population.^1,2 Among the factors thought to lead to this increased risk of cardiovascular events are the development of obesity and the metabolic syndrome.

Patients living with HIV in the era of effective ART are overweight or obese at rates similar to that of the general population and, as such, suffer from the associated comorbidities of hypertension and dyslipidemia.³ Risk factors for elevated body mass index (BMI) for women were similar between HIV-positive and -negative women in one study, with African American ethnicity being associated with significantly higher BMI.⁴ Besides the detrimental effects of the comorbid medical conditions associated with obesity, the development of body physical changes in those on ART can have negative psychosocial consequences and possibly impact treatment adherence as well.⁵ As such, HIV-associated central fat accumulation is becoming more of a problem for patients.⁶ While lifestyle modification is always reasonable, and switching ART to a nonprotease inhibitor-based regimen may be considered, it appears these options are of limited value in decreasing visceral adipose tissue.⁶

Agents used to treat diabetes mellitus, such as metformin and the thiazolidinediones, have been evaluated in clinical studies with inadequate results. Testosterone replacement has also not been shown to be effective in treating abdominal obesity in HIV infected individuals. There are some data to support the use of low-dose growth hormone replacement for the treatment of central fat accumulation in HIV-infected individuals who are growth hormone deficient. ⁶ Tesamorelin, a growth-hormone–releasing hormone analogue, has recently been approved to improve visceral adiposity, but its long-term effects are not yet known.⁷

Another potential option to reduce obesity and the metabolic dysregulation associated with excess weight in HIV-infected patients is bariatric surgery. The efficacy, safety, and durability of bariatric surgery for the treatment of obesity and cardiometabolic disease determinants, such as diabetes, hypertension, and dyslipidemia, have been documented in the general population.^8

–11 However, there are few data regarding the outcomes for those with HIV infection undergoing bariatric surgery. A previous case series of six morbidly obese patients with stable HIV disease who underwent Roux-en-Y gastric bypass (RYGB) reported that weight loss and resolution of obesity-related comorbidities were comparable to those in the general population who underwent gastric bypass surgery.¹² The authors noted that none of the patients had significant drops in CD4 cell counts or progression to AIDS during the study. However, supportive data regarding postoperative CD4 cell counts and viral loads were not provided. A separate report of two other HIV-infected patients who underwent gastric bypass surgery was recently published, although again without complete data regarding viral load suppression and ART management.¹³

It is important to determine the virologic and immunologic outcomes in patients undergoing bariatric surgery. Because the absorption and metabolism of antiretroviral therapies may be altered due to the surgery, it cannot be assumed that HIV treatment outcomes will be optimal. In addition, complications from surgery may result in prolonged interruptions in ART, thereby increasing the risk of faster HIV disease progression. Thus, we performed this analysis to better understand the HIV-related outcomes of patients undergoing bariatric surgery. We also examined changes in weight and metabolic parameters in this group.

Methods

We performed a retrospective case series analysis of seven HIV-infected patients who had bariatric surgery and received their HIV care at Wishard Memorial Hospital, Indiana University Hospital, Methodist Hospital, and one private practice HIV clinic, all in Indianapolis. There is no central database to identify all individuals with HIV who have had bariatric surgery. The subjects were identified by polling HIV caregivers in our academic referral center (n = 4) and at a large private practice (n = 3) in the Indianapolis area. The subjects' existing health care data from January 1, 1999 through October 31, 2009 were examined. Data abstraction began after this date.

Descriptive statistics (medians, ranges) were used for all continuous data. Categorical data were listed as simple proportions. This study was approved by the Indiana University Institutional Review Board. Because only existing medical records were used, informed consent was not required.

Results

Table 1 describes the characteristics of the seven subjects included in this case series. Three of the subjects were female. The median (range) age was 46 (33–50) years, and the median (range) time from HIV diagnosis to time of surgery was 10 (7–20) years. The median (range) CD4 cell count preoperatively was 682/mm³ (238–1626/mm³). All six of the subjects on ART preoperatively were virally suppressed (HIV-1 RNA <48 copies per milliliter). Five of those subjects remained virally suppressed after surgery. Subject 7 was virally suppressed preoperatively and continued to take ART postoperatively. However, this subject developed severe nausea 3 months after surgery, so her ART was held for 2 months. ART was resumed in this subject afterwards, but viral load and CD4 cell count testing during resumption of ART were not yet performed at the time of this analysis. Subject 5 was not on ART preoperatively with a CD4 cell count of 682/mm³. At postoperative months 3, 5, and 8, this subject's CD4 cell counts were 457/mm³, 408/mm³ and 226/mm³, respectively. This trend paralleled the reduction in BMI postoperatively from 51, 46, and 39 kg/m² at the same timepoints. ART was subsequently initiated using a regimen of tenofovir, emtricitabine, and ritonavir-boosted darunavir. Subject 5 subsequently became virally suppressed 3 months later with the most recent CD4 cell count being 397/mm³.

Table 1.

Characteristics of the Case Subjects

	Subject 1	Subject 2	Subject 3	Subject 4	Subject 5	Subject 6	Subject 7	Range
Age at time of surgery (years)	45	48	40	43	35	50	33	33–50
Gender	M	M	M	M	F	F	F
Race	C	C	C	C	C	C	C
Duration HIV diagnosis (years)	20	10	13	11	7	10	7	7–20
Duration of post-op follow-up	12 months	16 months	9 years	12 months^a	16 months	9 months	12 months	9 months–9 years
ART preoperative	Yes	Yes	Yes	Yes	No	Yes	Yes
ART regimen preoperative	TDF/FTC/RAL/DRV/r	TDF/FTC/EFV	dDI/d4T/EFV	TDF/FTC/EFV	NA	TDF/FTC/EFV	TDF/FTC/dDI/RAL/ETV
CD4 count, cells/mm³ [%]
Preoperative	238 [11]	624 [22]	690 [36]	1626 [53]	682 [31]	619 [33]	845 [37]	238-1626 [11–53]
Postoperative	266 [14]	712 [21]	947 [47]	908 [51]	226^b [18]	324 [17]	352 [28]	226-947 [14–51]
Change	28 [+3]	88 [−1]	257 [+11]	−718 [−2]	−456 [−13]	−295 [−16]	−493 [−9]	−718 to +257 [−13 to +11]
HIV viral load, copies/mL
Preoperative	<48	<48	<50	<48	4540	<48	<48	<48–4540
Postoperative	<48	<48	<50	<48	<48	<48	65,000^c	<48–65,000
Surgical complications	None	None	Hernia^d	None	Stenosis^e	Leak^f	None
Vitamin deficiency^g	NA	NA	NA	Yes	Yes	NA	Yes

Note: Preoperative data all within 4 months prior to surgery. Postoperative data are most recently available.

Had 1st bariatric surgery in 1999, lost 170lbs then gained back weight so had laparoscopic conversion of a vertical banded gastroplasty to a gastric bypass.

Started ART based on this CD4 cell count and subsequently became virally suppressed.

Was “missing some ART due to nausea” so ART held then later resumed but no new data available.

Developed post-operative ventral hernia that has required multiple surgeries and also had recurrent Staphylococcus aureus surgical site infections.

Re-admitted 4 days after surgery and taken back to operating room for corrective surgery.

Developed an anastomatic leak post-operatively, so could not take oral medication. Thus, ART was held for several months. Once ART resumed, viral suppression subsequently occurred.

Post-operatively; vitamin B₁, vitamin B₁₂, and folate.

Change: postoperative values minus preoperative values.

M, male; F, female; C, caucasian; ART, antiretroviral therapy; NA, not available or not applicable; TDF, tenofovirl; FTC, Emtricitabine; RAL, raltegravir; r, ritonavir; DRV, darunavir; dDI, didanosine; d4T, stavudine; EFV, efavirenz; ETV, etravirine.

Three of the seven subjects had surgical complications. Subject 3 developed a postoperative ventral hernia that required surgical repair 5 months postoperatively. He had multiple hernia repairs and recurrent Staphylococcus aureus surgical site wound infections. Subject 5 was readmitted 4 days after surgery and taken back to the operating room for presumed stenosis of the gastrojejunostomy. Subject 6 developed postoperative renal insufficiency due to acute tubular necrosis secondary to hypovolemia and subsequently required hemodialysis. This was followed by the development of an anastomotic leak. This subject's ART was held during this time period. After resolution of the leak, ART was resumed, and the subject became virally suppressed.

We were unable to ascertain whether obesity preceded HIV, ART or both due to incomplete records. The median (range) change in BMI postoperatively was −10 kg/m² (−6 to −28 kg/m²). There were data available for vitamin levels on only three of the subjects. Subject 5 developed vitamin B₁₂, folate, and vitamin B₁ deficiencies 9 months after surgery. Subject 7 developed vitamin B₁ deficiency 3 months after surgery. Subject 4 was noted to have a vitamin B₁₂ level on the lower end of normal range 5 months after surgery while receiving daily oral B complex and oral B₁₂ supplements.

The available data regarding metabolic comorbidities in this retrospective case series suggest improvements in these cardiovascular risk factors after bariatric surgery. Table 2 describes the changes in metabolic parameters with bariatric surgery. The median (range) change in triglycerides was −185 mg/dL (−739 to +35 mg/dL). The median (range) changes in total cholesterol, low-density lipoprotein (LDL) cholesterol, and high-density lipoprotein (HDL) cholesterol were −19 mg/dL (−61 to +3 mg/dL), −41 mg/dL (−63 to +18 mg/dL), and +11.5 mg/dL (+3 to +14 mg/dL), respectively. The median (range) changes in systolic blood pressure was and diastolic blood pressure were −4 mm Hg (−22 to +24 mm Hg) and +4 mm Hg (−5 to +19 mm Hg), respectively. The median (range) change in fasting serum glucose was −17 mg/dL (−32 to +6 mg/dL). Four of the subjects had reductions in their metabolic medication prescriptions post-operatively.

Table 2.

Changes in Metabolic Parameters with Bariatric Surgery

Characteristic	Subject 1	Subject 2	Subject 3	Subject 4	Subject 5	Subject 6	Subject 7	Range
BMI, kg/m²
Preoperative	35	38	50	48	58	40	55	35–58
Postoperative	29	28	35	39	30	30	33	28–35
Change	−6	−10	−15	−9	−28	−10	−22	−6 to −28
Metabolic medications
Preoperative	MET/FIB/SIM/EZE	MET/FIB/VAL/MTP	GLI/FIB/NIA	INS/GLI/MET/ATO	NA	NA	LIS
Postoperative	None	None	GLI/FIB/NIA	MET/ATO	None	None	None
Decreased pill burden^a	Yes	Yes	NA	Yes	NA	NA	Yes
Triglycerides (mg/dL)
Preoperative	1048	353	709	111	191	364	NA	111–1048
Postoperative	309	201	NA	146	NA	146	135	135–309
Change	−739	−152	NA	35	NA	−218	NA	−739 to +35
Total cholesterol (mg/dL)
Preoperative	244	188	250	155	189	201	NA	155–244
Postoperative	192	185	189	144	NA	182	134	134–192
Change	−52	−3	−61	−11	NA	−19	NA	−61 to −3
Low density lipoprotein-cholesterol (mg/dL)
Preoperative	NA	92	NA	93	120	128	124	92–128
Postoperative	104	110	NA	61	NA	78	61	61–104
Change	NA	18	NA	−32	NA	−50	−63	−63 to +18
High-density lipoprotein-cholesterol (mg/dL)
Preoperative	23	25	NA	40	31	31	NA	23–40
Postoperative	26	35	NA	54	NA	44	46	26–54
Change	3	10	NA	14	NA	13	NA	3–13
Systolic blood pressure (mm Hg)
Preoperative	128	120	150	130	128	126	142	120–150
Postoperative	124	128	174	108	124	127	135	108–174
Change	−4	8	24	−22	−4	1	−7	−22 to +24
Diastolic blood pressure (mm Hg)
Preoperative	81	82	80	76	76	70	81	70–82
Postoperative	78	86	99	78	92	81	76	76–99
Change	−3	4	19	2	16	11	−5	−5 to +19
Fasting serum glucose (mg/dL)
Preoperative	97	75	136	96	84	114	98	75–136
Postoperative	79	79	104	94	90	89	81	79–104
Change	−18	4	−32	−2	6	−25	−17	−25 to +4

Note: preoperative data all within 4 months prior to surgery. Postoperative data are most recently available.

Change: Postoperative values minus preoperative values.

Decreased pill burden for diabetes mellitus, dyslipidemia, or hypertensive medications.

NA, not available; BMI, body mass index; MET, metformin; FIB, fenofibrate; SIM, simvastatin; EZE, ezetimibe; VAL, valsartan; MTP, metoprolol; GLI, glipizide; ATO, atorvastatin; LIS, lisinopril.

Discussion

This case series represents the first report of virologic and immunologic outcome data of HIV-infected patients who have undergone bariatric surgery. Based on this retrospective analysis, it appears that bypass surgery may be an effective treatment modality for obesity and its related comorbidities in this specific population for those that have failed more conservative therapy.

Among the four subjects who were virally suppressed on ART prior to surgery and did not have any treatment interruptions, viral suppression was maintained postoperatively. The CD4 cell counts were preserved in three of these four subjects. While one of these subjects (subject 4) saw a decrease in his CD4 cell count, his CD4% remained above 50% postoperatively. The dosages of ART were not changed postoperatively in any of the patients. Thus, we can surmise bariatric surgery did not significantly alter the absorption of the antiretroviral drugs used in these individuals. It was interesting to note that the one subject who was not on ART with a CD4 cell count of 682/mm³ prior to surgery experienced a rapid decrease in CD4 cell count to 226/mm³ 8 months after surgery. This trend paralleled the reduction in BMI to 39 kg/m². The drop in CD4 cell counts in this subject is similar to that reported in one previous description of an ART-naïve patient who underwent bariatric surgery.¹³ That patient had a preoperative CD4 cell count of 368/mm³. Six months after surgery, the patient was admitted to the hospital with seizures and found to have a drop in her CD4 cell count to 291/mm³. The etiology of the seizure was not reported, though the patient was started on antiseizure medication.

The effect of weight loss on immunologic function after bariatric surgery has not yet been clearly defined. Several studies have demonstrated that obesity is associated with higher and more stable CD4 cell counts and may result in slower progression of HIV disease to AIDS.^14
–16 However, these studies primarily included subjects not receiving ART. More recent data suggest that higher BMI may negatively affect CD4 count recovery.¹⁷ The rapid reduction in CD4 cell count observed after bariatric surgery in the patient we described who was not receiving ART is likely to be multifactorial. One possibility may be related to nutritional deficiencies commonly found after bariatric surgery. Nutritional deficiencies can occur after bariatric surgery due to both inadequate intake as well as anatomical changes that effect absorption of micronutrients.¹⁸ Low vitamin B₁₂ levels have been postulated to lead to faster rates of HIV disease progression.¹⁹ While the data regarding vitamin levels were incomplete in our study, several subjects did have nutritional deficiencies postoperatively. Subject 5, who was not on ART preoperatively, experienced a precipitous drop in her CD4 cell count from 682/mm³ preoperatively to 226/mm³ 8 months after surgery. This coincided with the development of vitamin B₁₂, folate and vitamin B₁ deficiency 9 months after surgery. Current recommendations include supplementation with vitamins B₁ and B₁₂, folate, iron, calcium, vitamin D and K after bariatric surgery.²⁰ Given our data, these recommendations to monitor and supplement for micronutrient deficiencies may have important immunologic consequences.¹⁹

Indications for bariatric surgery include a BMI >40 kg/m² or a BMI >35 kg/m² along with the presence of serious comorbidities such as diabetes mellitus (DM), sleep apnea, obesity-related cardiomyopathy, or severe joint disease.²¹ The seven subjects in our study had a median decrease in BMI of 10 kg/m² (range, 6–28 kg/m²) postoperatively. Only one of the two prior case series mentioned above reported BMI data. The first patient's BMI was 42 kg/m² preoperatively and then decreased to 28 kg/m² 30 months after surgery.¹³ The second patient had a BMI of 54 kg/m² preoperatively which then decreased to 38 kg/m² 18 months after surgery. The improvement in BMI seen in our subjects is similar in magnitude to the weight loss observed in a large cohort study of HIV-negative individuals followed over 2 years after bariatric surgery.⁸

In our case series, five of the seven subjects postoperatively were not taking any medications for dyslipidemia or DM. None of the seven subjects were taking blood pressure medications postoperatively. Four subjects (1, 2, 4, 7) were able to decrease their pill burden postoperatively (Table 2). The improvement in obesity-related comorbidities was similar to that reported in a prior study of HIV-positive subjects who underwent bariatric surgery.¹² In that series of six patients, all three of the subjects with DM preoperatively no longer required hypoglycemic drug therapy after surgery. In this other series, one of the two subjects with hypertension no longer required medication postoperatively and the second subject was able to reduce their dosage. For the two subjects with dyslipidemia, one no longer required medication and the other was able to reduce their dosage postoperatively. Thus, it appears that metabolic comorbidities are ameliorated after bariatric surgery in those infected with HIV, similar to the general population who undergo this procedure.⁸

In our series, three of the seven subjects experienced a surgical complication. Stenosis at the gastrojejunostomy has been reported as a complication in 4.9% of uninfected subjects in one large study whereas anastomotic leak has been reported in 1.7% of such subjects.^22,23 Hernia development was reported as a complication in 2.5% of HIV-negative subjects in a large study.²² While increased surgical complication rates have been associated with CD4 cell counts less than 50/mm³, there are no data currently to suggest that people with HIV and preserved CD4 counts are at higher risk for surgical complications.²⁴ Of note, one subject had a delay in reinitiating therapy due to prolonged nausea and vomiting after surgery. Postoperative nausea and vomiting after gastric bypass can be due to multiple etiologies including maladaptive dietary patterns, marginal ulcers at the anastomosis, or stomal stricture at the gastrojejunal anastomosis.^22,23 The etiology of this subject's nausea was never fully defined. There were no data from our cases to suggest virologic failure or development of resistance due to planned or unplanned treatment interruptions perioperatively. However, this does highlight the need to consider staggered discontinuation of ART regimens that contain a component with a longer half-life such as efavirenz, as well as potential alternative regimens in liquid form were the patient not able to tolerate the pill form post-operatively. While the eight patients previously reported in the surgical literature did not have any surgical complications,^12,13 we observed complications in three of the seven patients we report in this case series. The significance of this is unclear due to the small sample size and the recall bias inherent in our case ascertainment. Thus, the complication rate seen in this series may not be a valid estimate. Clearly, larger studies are needed to define more fully the risk of bariatric surgery complications in the HIV-infected population.

We conclude that bariatric surgery may be an effective and reasonable treatment modality for obesity and its related comorbidities in people living with HIV infection who have failed more conservative therapy with diet and therapeutic lifestyle changes. Large-scale studies are needed to determine surgical complication rates in this population, assess the impact of bariatric surgery on CD4 cell counts in those that are not on ART preoperatively as well as confirm our findings that viral suppression preoperatively is durable in those receiving ART.

Footnotes

Acknowledgments

None of the authors declare any conflict of interest.

Author Disclosure Statement

No competing financial interests exist.

References

Hsue

, Hunt

, Schnell

et al. Role of viral replication, antiretroviral therapy, and immunodeficiency in HIV-associated atherosclerosis. AIDS, 2009; 23:1059–1067.

Boccara

. Cardiovascular complications and atherosclerotic manifestations in the HIV-infected population: Type, incidence and associated risk factors. AIDS, 2008; 22,suppl 3:S19–S26.

Crum-Cianflone

, Tejidor

, Medina

et al. Obesity among patients with HIV: The latest epidemic. AIDS Patient Care STDs, 2008; 22:925–930.

Boodram

, Plankey

, Cox

et al. Prevalence and correlates of elevated body mass index among HIV-positive and HIV-negative women in the Women's Interagency HIV Study. AIDS Patient Care STDs, 2009; 23:1009–1016.

Cabrero

, Griffa

, Burgos

et al. Prevalence and impact of body physical changes in HIV patients treated with highly active antiretroviral therapy: Results from a study on patient and physician perceptions. AIDS Patient Care STDs, 2010; 24:5–13.

Cofrancesco

, Freedland

, McComsey

. Treatment options for HIV-associated central fat accumulation. AIDS Patient Care STDs, 2009; 23:5–18.

Falutz

, Allas

, Blot

et al. Metabolic effects of a growth hormone-releasing factor in patients with HIV. N Engl J Med, 2007; 357:2359–2370.

Sjostrom

, Lindross

, Peltonen

et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med, 2004; 351:2683–2693.

Sjostrom

, Narbro

, Sjostrom

et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med, 2007; 357:741–752.

10.

Adams

, Gress

, Smith

et al. Long-term mortality after gastric bypass surgery. N Engl J Med, 2007; 357:753–761.

11.

The Longitudinal Assessment of Bariatric Surgery (LABS) Consortium. Perioperative Safety in the Longitudinal Assessment of Bariatric Surgery. N Engl J Med, 2009; 361:445–454.

12.

Flancbaum

, Drake

, Colarusso

et al. Initial experience with bariatric surgery in asymptomatic human immunodeficiency virus-infected patients. Surg Obes Relat Dis 1, 2005; 73–76.

13.

Fazylov

, Soto

, Merola

. Laparoscopic gastric bypass surgery in human immunodeficiency virus-infected patients. Surg Obes Relat Dis, 2007; 3:637–639.

14.

Shor-Posner

, Campa

, Zhang

et al. When obesity is desirable: A longitudinal study of the Miami HIV-1-infected drug abusers (MIDAS) cohort. J Acquir Immune Defic Syndr, 2000; 23:81–88.

15.

Shuter

, Chang

, Klein

. Prevalence and predictive value of overweight in an urban HIV care clinic. J Acquir Immune Defic Syndr, 2001; 26:291–297.

16.

Jones

, Hogan

, Snyder

et al. Overweight and human immunodeficiency virus progression in women: associations between HIV disease progression and changes in body mass index in women in the HIV Epidemiology Research Study cohort. Clin Infect Dis, 2003; 37,suppl:S69–80.

17.

Crum-Cianflone

, Roedigera

, Eberlya

et al. The Infectious Disease Clinical Research Program HIV Working Group. Obesity among HIV-infected persons: Impact of weight on CD4 cell count. AIDS, 2010; 24:1063–1075.

18.

Bloomberg

, Fleishman

, Nalle

et al.

Nutritional deficiencies following bariatric surgery: What have we learned?

Obes Surg, 2005; 15:145–154.

19.

Tang

, Graham

, Chandra

et al. Low serum vitamin B-12 concentrations are associated with faster Human Immunodeficiency Virus Type 1 (HIV-1) disease progression. J. Nutr, 1997; 127:345–351.

20.

Mechanick

, Kushner

, Sugerman

et al. American Association of Clinical Endocrinologists, The Obesity Society, and American Society for Metabolic & Bariatric Surgery Medical guidelines for clinical practice for the perioperative nutritional, metabolic, and nonsurgical support of the bariatric surgery patient. Obesity, 2009; 17,Suppl 1:1.

21.

NIH Conference. Gastrointestinal surgery for severe obesity. Consensus Development Conference Panel. Ann Intern Med, 1991; 115:956–961.

22.

Higa

, Boone

, Ho

. Complications of the laparoscopic Roux-en-Y gastric bypass: 1,040 patients—what have we learned? Obes Surg, 2000; 10:509–513.

23.

Papasavas

, Hayetian

, Caushaj

et al. Outcome analysis of laparoscopic Roux-en-Y gastric bypass for morbid obesity. The first 116 cases. Surg Endosc, 2002; 16:1653–1657.

24.

Horberg

, Hurley

, Klein

et al. Surgical outcomes in human immunodeficiency virus–infected patients in the era of highly active antiretroviral therapy. Arch Surg, 2006; 141:1238–1245.