Indian J Gastroenterol DOI 10.1007/s12664-015-0537-8

ORIGINAL ARTICLE

Gastrointestinal complications in renal transplant recipients detected by endoscopic biopsies in a developing country Muhammed Ishaque & Rahma Rashid & Muhammed Mubarak

Received: 7 August 2014 / Accepted: 5 January 2015 # Indian Society of Gastroenterology 2015

Abstract Background Renal transplantation is the treatment of choice for patients with end-stage renal disease. The renal transplant recipients are susceptible to a variety of gastrointestinal (GI) complications such as infections, ulcer disease, and malignancies. Objectives We aimed to determine the frequency of pathological lesions in GI endoscopic biopsies in recipients of live related renal transplantation in our setting. Methods This retrospective survey was carried out at Histopathology Department of Sindh Institute of Urology and Transplantation, Karachi, from December 2010 to January 2011. All consecutive renal transplant patients of all ages and both genders on regular follow up, presenting with GI complaints and in whom GI endoscopic biopsies were performed, were included. The demographic, clinical, and laboratory data were retrieved from case files and the pathological diagnoses from the original biopsy reports. Results A total of 200 consecutive renal transplant patients were enrolled. The biopsies comprised of 19 (9.5 %) esophageal biopsies, 119 (59.5 %) gastric biopsies, 148 (74 %) duodenal biopsies, and 66 (33 %) colorectal biopsies. The main pathological lesions included cytomegalovirus infection in 22 (11 %) of all patients, Helicobacter pylori in 11 (9.2 %) of gastric biopsies, cryptosporidium in 4 (1.6 %), giardiasis in 30 (15 %), immunoproliferative small intestinal disease in 5 (3.4 %), tropical sprue in 33 (15 %), tuberculosis in 3 (2 %) of the small intestinal biopsies, and gastric adenocarcinoma in 1 (1.7 %) gastric biopsy. Conclusion A wide spectrum of pathological lesions including opportunistic infections was seen in GI endoscopic M. Ishaque : R. Rashid : M. Mubarak (*) Javed I. Kazi Department of Histopathology, Sindh Institute of Urology and Transplantation, Karachi, Pakistan e-mail: [email protected]

biopsies in renal transplant patients. Endoscopic biopsies play an important role in the diagnosis and management of GI disease in renal transplant patients. Keywords Endoscopic biopsies . Immunosuppression . Opportunistic infections . Pathological lesions . Renal transplant recipients

Introduction Renal transplantation is the treatment of choice in patients with end-stage renal disease (ESRD) [1]. With improved transplantation technology and new immunosuppressive agents, 1-year survival rates for grafts are reported to be >90 %. However, the long-term outcome has not improved substantially during the last few decades [2]. The allo-transplantation and the consequent immunosuppression lead to a variety of complications involving not only the allograft but various other native organs and systems of the recipient. Several factors, such as the cause of terminal uremia, immunosuppressive medications, and infections, can predispose kidney transplantation patients to the development of gastrointestinal (GI) complications. A wide range of both medical and surgical GI complications such as infections, ulcer disease, and malignancies can occur [3–7]. The diagnosis of severe GI complications can be delayed, and treatment can be more complicated due to the use of immunosuppressive medications [8]. These pose considerable diagnostic and therapeutic challenges to the transplant physicians, surgeons, and gastroenterologists who care for these patients. The frequency of GI complications in renal transplant patients is relatively high, ranging from 10 % to 20 %, and may lead to graft loss and even patient death [3]. It has been

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observed that most of the GI complications occur during the first posttransplant year, when the doses of immunosuppressive drugs are highest [4]. A number of GI complications such as herpetic esophagitis (2.2 %), cytomegalovirus (CMV) infection (12.5 %), giardiasis (1.4 %), tropical sprue (18.8 %), Helicobacter pylori-associated gastritis (30 %), peptic ulcer disease (42 %), cryptosporidiosis (11.5 %), lymphomas (6.3 %), and abdominal tuberculosis (12.6 %) may affect gastrointestinal tract (GIT) in these patients [4, 9–13]. Definitive diagnoses of these require detailed history, physical examination, endoscopy, and biopsy. The advent of fiberoptic endoscopic procedure has revolutionized the approach to the diagnosis and management of medical conditions involving the GIT. This allows direct visualization of the lesions and sampling of appropriate sites for the histopathological examination. There is very little data on the spectrum of pathological lesions in endoscopic biopsies of GIT in renal transplant patients in the available literature. Almost all of the reported studies have been clinical-, endoscopy-, or autopsy-based [3–7, 14–19]. Most of the reported studies have been carried out in cadaveric renal transplant recipients. Only sporadic studies are available on the medical complications involving GIT in renal transplant patients in live-related renal transplant patients [4]. This study was an attempt to determine the magnitude of pathological lesions in GI biopsies of live-related renal transplant patients presenting with various GI complaints in our setting.

Pathological study The endoscopic biopsy samples were fixed in 10 % buffered formalin and processed and paraffin embedded. Sections were cut and stained by hematoxylin and eosin (H&E), Alcian blue–periodic acid–Schiff (AB-PAS) and any other special stains as and when needed. Giemsa staining was done routinely on all gastric biopsies for the detection of H. pylori infection. The sections were examined under the light microscope (LM) and pathological diagnosis made by two consultant histopathologists with 10 and 20 years experience, first independently and then jointly to arrive at a consensus diagnosis. Pathological definitions Tropical sprue (TS) was diagnosed when there was variable villous blunting associated with crypt hyperplasia, increased numbers of chronic inflammatory cells in the lamina propria, and increased intraepithelial lymphocytes (IEL). The negative serology for celiac disease differentiated TS from glutensensitive enteropathy (GSE). Sprue was differentiated from the chronic nonspecific duodenitis mainly on the basis of IEL counts on duodenal biopsy, the latter being normal or only minimally increased in chronic nonspecific duodenitis and also correlation with clinical presentation. Collagenous colitis was diagnosed when there was markedly thickened subepithelial collagen layer demonstrated on trichrome stain and increased numbers of chronic inflammatory cells in the lamina propria and surface epithelium accompanied by denegerative changes in the surface epithelial cells [20].

Methods Data analysis This was a retrospective, cross-sectional, and descriptive study carried out in the Histopathology Department of Sindh Institute of Urology and Transplantation (SIUT), Karachi, from December 2010 to January 2011. All consecutive renal transplant patients of all age groups and both sexes on regular follow up at Transplant OPD, SIUT, presenting with GI complaints such as vomiting, dyspepsia, diarrhea, weight loss, rectal bleeding, and in whom GI diseases were suspected and GI biopsies performed were included. The following cases were excluded: (1) dietary factors or psychological factors such as anorexia nervosa, (2) patients with systemic diseases such as posttransplant diabetes and pulmonary tuberculosis, and (3) renal transplant patients with GI complications but in whom no endoscopic biopsies were performed. Informed consent was obtained from all patients and parents of children before undertaking the endoscopic procedure and the biopsies. Demographic and clinical data were collected from clinical charts of patients. Pathological diagnoses on endoscopic biopsies of these patients were noted from the original biopsy reports.

The data were analyzed using the Statistical Package for Social Sciences (SPSS) version 10.0 computer program (SPSS, Chicago, IL, USA). Mean±SD and median (with range) were used for continuous variables such as age. Numbers (percentages) were used for categorical data such as gender and frequencies of various pathological lesions in GI endoscopic biopsies. Comparison among the groups was made using chi-square test, and p< 0.05 was considered significant.

Results Out of the 2,500 kidney transplant patients on regular followup, 200 (8 %) patients presented with GI complications during the follow up in the median posttransplant duration of 35.23± 3.0 months (range, 23 days to 11 years) after kidney transplantation. Out of these, 171 (85.5 %) were male and 29 (14.5 %) were female with male/female ratio of 6:1. The mean±SD age

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of all patients was 32.03±10.0 years (range, 13–58 years). The majority of patients belonged to 20–40 years age group. The vast majority of the renal transplant patients had positive CMV serology; only four (2 %) were negative for CMV prior to transplantation. All patients were on triple drug immunosuppressive regimen with different combinations of drugs. Of these, 198 (99 %) were on steroids, 183 (81.5 %) on cyclosporine, 158 (79 %) on azathioprine, 42 (21 %) on mycophenolate mofetil (MMF), and 17 (8.5 %) on tacrolimus. Regarding the primary cause of ESRD, it was unknown in the majority of cases: 143 (71.5 %) of the patients. Chronic sclerosing glomerulonephritis (GN) was found in 19 (9.5 %) patients, followed by stone disease in 18 (9 %) and hypertensive nephropathy in 10 (5 %) patients. Other causes of renal failure were adult polycystic kidney disease (APCKD) in four (2 %), focal segmental glomerulosclerosis (FSGS) in two (1 %), neurogenic bladder in two (1 %), diabetic nephropathy in one (0.5 %), and Fabry’s disease in one (0.5 %). Regarding GI complaints, 116 (58 %) patients had diarrhea, 87 (43.5 %) weight loss, 34 (17 %) epigastric pain, per rectal bleeding in 18 (9 %), dyspepsia in 17 (8.5 %), vomiting in 6 (3 %), constipation in 4 (2 %), and fever in 4 (2 %). Table 1 shows the main indications of performing GI endoscopic biopsies in these patients. The GI biopsies were performed at a median posttransplant duration of 27.3 months [interquartile range (IQR), 8.3–42.6 months]. In 81.5 % of cases, the biopsies were done within first 5 years posttransplantation (Fig. 1), and in 58 (29 %) of cases, the biopsies were done within first year posttransplantation. Regarding the biopsies and pathological lesions, esophageal biopsies were done in 19 (9.5 %) patients. Among these, reflux esophagitis was found in 10 (52.63 %) biopsies, CMV infection in 4 (21.05 %), Barrett’s esophagus in 4 (21.05 %), and esophageal cadidiasis in 3 (15.8 %), as shown in Table 2. One case of esophageal candidiasis was seen in isolation, one in association with CMV esophagitis, and one with Barrett’s esophagus. Gastric biopsies were done in 119 (59.5 %) patients, and the pathological diagnoses included reflux gastropathy in 51 Table 1 Frequency of different gastrointestinal signs and symptoms in 200 renal transplant patients Signs and symptoms

Numbers

Percentage

Diarrhea Weight loss Epigastric pain Bleeding per rectum Dyspepsia Vomiting Fever Constipation

116 87 34 18 17 6 4 4

58 43.5 17 9.0 8.5 3.0 2.0 2

Fig. 1 Histogram showing the number of gastrointestinal biopsies done according to posttransplant duration in years

(42.85 %) cases, followed by chronic nonspecific gastritis in 43 (36.13 %) patients. H. pylori-associated chronic active gastritis was found in 11 (9.24 %) cases, CMV gastritis in 7 (5.88 %), chronic active nonspecific gastritis in 3 (2.52 %), follicular gastritis in 2 (1.68 %), chronic gastritis with intestinal metaplasia in 1 (0.84 %), and gastric adenocarcinoma in 1 (0.84 %) patient with gastric biopsies, as shown in Table 3. Duodenal biopsies were done in 148 (74 %) patients. Chronic nonspecific duodenitis was diagnosed in 65 (43.91 %) patients, tropical sprue in 33 (22.29 %), giardiasis in 29 (19.59 %), erosive duodenitis in 7 (4.72 %), IPSID in 5 (3.37 %), cryptosporidiosis in 4 (2.75 %), combined cryptosporidiosis and giardiasis in 1 (0.68 %), small intestinal tuberculosis in 3 (2.02 %), and CMV duodenitis in 1 (0.68 %) of the duodenal biopsies, as shown in Table 4. All five cases of IPSID were of early stage. The biopsies were done at a mean posttransplant duration of 45.8±44.7 months (range, 7.9– 122.2 months). All patients were male with a mean age of 31.8±9.8 years. The biopsies demonstrated moderate villous stunting, diffuse infiltration of plasmacytic cells limited to the lamina propria, and a paucity of crypts. No lymphoepithelial lesions or lymphoid follicles were seen, nor extension into the submucosa. Colonic biopsies were performed in 50 (25 %) patients. Among these, 34 (68 %) patients were found to have chronic nonspecific colitis, 9 (18 %) patients had CMV colitis, 6 Table 2 Biopsy findings in 19 renal transplant patients who underwent esophageal biopsies Pathological lesions

Numbers

Percentage

Reflux esophagitis Barrett’s esophagus Cytomegalovirus esophagitis Candida infection

10 4 4 3

52.63 21.05 21.05 15.8

Indian J Gastroenterol Table 3 Frequency distribution of different gastric lesions detected on endoscopic biopsies in 119 renal transplant recipients

Table 5 The biopsy findings in 50 renal transplant patients who underwent colonic biopsies

Pathological lesions

Number

Percentage

Pathological lesions

Numbers

Percentage

Reflux gastropathy Chronic nonspecific gastritis H. pylori-associated gastritis Cytomegalovirus gastritis

51 43 11 7

42.85 36.13 9.24 5.88

Chronic nonspecific colitis Cytomegalovirus colitis Chronic active nonspecific colitis Collagenous colitis

34 9 6 1

68 18 12 02

3 2 1 1

2.52 1.68 0.84 0.84

Chronic active nonspecific gastritis Follicular gastritis Adenocarcinoma Chronic gastritis with metaplasia

(12 %) had chronic active nonspecific colitis and 1 (2 %) had collagenous colitis, as shown in Table 5. Rectal biopsies were done in 16 (8 %) patients. Of these, eight (50 %) patients were diagnosed as chronic nonspecific proctitis, five (31.5 %) had chronic active nonspecific proctitis, two (12.5 %) had CMV proctitis, and remaining one (6.25 %) patient was diagnosed as solitary rectal ulcer, as shown in Table 6. The distribution of pathological lesions according to posttransplant duration was analyzed with an arbitrary cut-off point of 1 year to see the differences in the spectrum of pathological lesions. There were significant differences in the overall distribution of gastric and duodenal lesions according to the posttransplant duration (p-values, 0.008 and 0.012, respectively). However, there were no significant differences in the distribution of pathological lesions of esophageal, colonic, or rectal biopsies. In addition, CMV infection was more common in early biopsies (1 year). No correlation of the pathological lesions with overall biopsy duration or endoscopic findings was found (results not shown). Some representative lesions of the biopsies are shown in Figs. 2 and 3.

Table 4 Frequency distribution of pathological lesions in 148 patients who underwent duodenal biopsies Pathological lesions

Numbers

Percentages

Chronic nonspecific duodenitis Tropical sprue Giardiasis Erosive duodenitis Immunoproliferative small intestinal disease Cryptosporidiosis Tuberculosis Cytomegalovirus duodenitis Giardiasis and cryptosporidiosis

65 33 29 7 5 4 3 1 1

43.91 22.29 19.59 4.72 3.37 2.75 2.02 0.68 0.68

Discussion In this study, 200 patients who presented with GI complaints and in whom GI endoscopic biopsies were performed were included. All kidney transplantations were performed at our center, and all received kidneys from live-related donors. These patients were screened for different diseases before transplantation according to the established recommendations. Renal transplant recipients are susceptible to a wide variety of disease processes, both in the graft and in native organs/ systems of the body [21]. GI system is also one of the commonly affected systems in these patients. Many studies have been published in international literature, highlighting the susceptibility of GI system in these patients [22]. However, there is no information in local literature on GI complications in renal transplant patients from Pakistan. Out of the 2,500 renal transplant patients on regular followup at our center, 200 patients presented with GI complications during the study period of 1 year. The frequency of GI complications in our setting was low as compared to earlier studies (8 % vs. 8 % to 37 % [23]. It has been observed that most of the GI complications occur during the first posttransplant year, when the doses of immunosuppressive drugs are highest [21, 22]. In our study, too, 58 (29 %) patients had GI complications in the first posttransplant year. Our results indicate that small intestinal involvement is most common in renal transplant patients. Out of the 200 patients, 148 (74 %) had biopsy proven small intestinal pathology. Tropical sprue was the most common specific pathology of the small intestine seen in 33 (22.29 %) of the patients. In a north Indian series, only 2 out of 166 patients suffered from malabsorption syndrome due to tropical sprue [24]. We

Table 6 Frequency of pathological lesions in rectal biopsies in 16 renal transplant patients Pathological lesions

Numbers

Percentage

Chronic nonspecific proctitis Chronic active nonspecific proctitis Cytomegalovirus proctitis Solitary rectal ulcer

8 5 2 1

50 31.25 12.5 6.25

Indian J Gastroenterol Fig. 2 a High power view showing severe H. pylori infection (Giemsa, ×1000). b Gastric antral biopsy showing extensive goblet cell metaplasia of the stomach (Alcian Blue– periodic acid–Schiff, ×200). c Duodenal biopsy showing moderate villous stunting and increased intraepithelial lymphocytes in tropical sprue (hematoxylin and eosin, ×400). d High-power view showing severe Giardia lamblia infection (hematoxylin and eosin, ×1000)

had significant number of patients with malabsorption due to a variety of causes. Majority of these patients were diagnosed as tropical sprue. Infective diarrheas are the most common cause of morbidity and mortality among the general population in developing countries, reflecting the poor sanitary conditions and low standard of life. This is also reflected in the renal transplant patient population in developing countries [10, 11, 25]. Among 200 patients, 116 (58 %) renal transplants patients in this series, had at least one episode of a diarrheal illness. Thirty-four (17 %) patients were affected by the parasitic infections. Of these, Giardia lamblia infection was found in 29 (14.5 %) patients, cryptosporidial infection in 4 (2 %) and Fig. 3 a Duodenal biopsy showing moderate villous stunting, moderate lymphoplasmacytic infiltrate with predominance of plasma cells and a relative paucity of crypts in a case of early immunoproliferative small intestinal disease (hematoxylin and eosin, ×100). b Duodenal biopsy showing heavy cryptosporidial infection (Giemsa, ×1000). c Duodenal biopsy showing well formed epithelioid granulomata consistent with tuberculosis (hematoxylin and eosin, ×400). d High-power view of colonic biopsy showing inclusions of cytomegalovirus infection in endothelial cells (hematoxylin and eosin, ×400)

combined G. lamblia and cryptosporidial infection in 1 (0.5 %) of all biopsied patients. Of course, all the above parasitic infections were detected on duodenal biopsies. The incidence of tuberculosis among live-related renal transplants ranges from 0.5 % to 1.0 % in North America to 9.5 % in our neighboring country, India [26, 27]. In endemic areas, it is probably secondary to the reactivation after immunosuppressive therapy, and most of the cases present within the first few months. We had three (2.02 %) patients with small intestinal tuberculosis. A high index of suspicion is required; abdominal tuberculosis should be suspected in patients with pyrexia of unknown origin, unexplained abdominal symptoms, and

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weight loss, especially if there is an abnormal chest X-ray finding. Transplant candidates should be thoroughly screened for tuberculosis and patients with latent disease or high risk should be treated prophylactically for 3–6 months [28]. Remaining transplant patients showed erosive duodenitis in seven (4.72 %) and IPSID in five (3.37 %) of duodenal biopsies. Only one patient had CMV duodenitis, while the rest of the patients had chronic nonspecific duodenitis. Our index of suspicion for the diagnosis of IPSID has been high, and we diagnosed five cases of IPSID at early stage, and these responded favorably to antibiotic therapy during the shortterm follow up period. Esophagitis in renal transplant recipients is mostly secondary to opportunistic infections by Candida, fungus, Herpes simplex, CMV, and rarely due to reflux disease [29]. Candidal esophagitis was the commonest esophageal disorder in renal transplant recipients in an earlier study [19]. This usually occurs within first 6 months after transplantation. Three (15.8 %) out of 19 transplant patients had developed candida fungal infection, a figure slightly higher than the previously reported incidence of 0.7 % to 5 % [30]. CMV esophagitis occurs most frequently after intense immunosuppression therapy or after rejection treatment. In this study, four (21.05 %) patients had CMV esophagitis, four (21.05 %) patients had Barrett’s esophagus, and ten (52.63 %) patients had esophagitis due to reflux disease. Many renal transplant patients may suffer from nausea, vomiting, abdominal pain, or gastric discomfort. These symptoms may be due to the numerous immunosuppressive pills some patients have to take daily. Nausea, vomiting, dyspepsia, and anorexia are particularly frequent in patients, who are on MMF, and are related to the doses of the drug and to the peak concentration in the blood [9]. H. pylori is the most common cause of gastritis and peptic ulcer disease in general population. The prevalence of H. pylori infection was 60 % to 70 % in renal transplant and hemodialysis patients, respectively, in a previous study conducted by Ozgur et al. [24]. In this study,11 (9.24 %) patients had H. pylori-associated gastritis, and 51 (42.85 %) patients had reflux gastropathy. CMV gastritis had been found in seven (5.88 %) patients, which was less frequent as compared to a previous Hungarian study [31]. Other causes of gastritis were chronic nonspecific gastritis, acute on chronic nonspecific gastritis, and follicular gastritis. The risk of gastric cancer is not increased in transplant patients. The risk of colonic cancer and anal canal cancer in transplant patients are much higher than in the general population [32–34]. In this study, we found a case of gastric adenocarcinoma in a renal transplant patient. However, no case of colonic or rectal malignancy was found. This may be due to the small sample size and short duration of the study period. Colonic complications in renal transplant patients are commonly seen. Most of the patients present with diarrhea, per rectal bleeding, weight loss, and constipation. Colonic

complications frequently occur in old age patients and patients with polycystic kidney disease as primary disease [8, 13]. Colonic perforation, largely caused by CMV infection, diverticulitis, immunosuppressive medications, nonsteroidal antiinflammatory drugs (NSAIDs), and malignancy had been reported in previous study of Stelzner et al. [8]. We found nine patients (18 %) of CMV colitis, presenting with per rectal bleeding and diarrhea. Other causes of colitis in transplant patients who presented with diarrhea, were collagenous colitis, chronic active nonspecific colitis, and chronic nonspecific colitis. There are certain limitations in the study. It originates from a single center and is a cross-sectional survey. Hence, no follow up on treatment response to specific forms of treatment is provided. The study also does not include all GI complications in these patients. We aim to carry out along with our clinical colleagues a more comprehensive study in near future to address the above shortcomings. In conclusion, a variety of pathological lesions including opportunistic infections are seen in GI endoscopic biopsies in renal transplant patients. These biopsies play an important role in the diagnosis and management of GI disease in renal transplant patients.

Conflict of interest MI, RR, and MM declare that they have no conflict of interest. Ethical statement The study was performed in a manner to conform with the Helsinki Declaration of 1975, as revised in 2000 and 2008 concerning Human and Animal Rights, and the authors followed the policy concerning Informed Consent as shown on Springer.com

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Gastrointestinal complications in renal transplant recipients detected by endoscopic biopsies in a developing country.

Renal transplantation is the treatment of choice for patients with end-stage renal disease. The renal transplant recipients are susceptible to a varie...
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