© 2015 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd Transplant Infectious Disease, ISSN 1398-2273
Case report
Bartonella henselae infection-associated vasculitis and crescentic glomerulonephritis leading to renal allograft loss A.R. Chaudhry, M.R. Chaudhry, J.C. Papadimitriou, C.B. Drachenberg. Bartonella henselae infection-associated vasculitis and crescentic glomerulonephritis leading to renal allograft loss. Transpl Infect Dis 2015: 17: 411–417. All rights reserved Abstract: Bartonella henselae (BH) is the main cause of cat scratch disease (CSD), which more typically presents as a self-limited localized suppurative lymphadenopathy in immunocompetent individuals. In contrast, immunocompromised patients commonly have systemic disease with life-threatening complications. In addition to the angioproliferative lesions, such as bacillary angiomatosis, an increasing number of immune post-infectious complications are being recognized with BH infections, including glomerulonephritis, vasculitis, hemophagocytic syndrome, and neurological problems. We report the case of a renal transplant recipient who developed CSD in the second year post transplantation. In addition to prolonged fever and generalized lymphadenopathy and splenomegaly requiring differentiation from a post-transplant lymphoproliferative disorder, the course was complicated by the development of dermal leukocytoclastic vasculitis and pauci-immune necrotizing and crescentic glomerulonephritis, which led to failure of the renal graft. Glomerulonephritis as a complication of CSD has never been described in a kidney allograft, to our knowledge. Awareness of the diverse clinical symptoms associated with BH, including granulomatous/suppurative lesions and other less common complications can lead to more rapid and accurate diagnosis. Also, as recommended by the current guidelines, a thorough history of pet ownership should be part of the clinical evaluation before and after transplantation for all transplant recipients.
First described by Debr e in 1950 (1), cat scratch disease (CSD) is the most common clinical syndrome related to Bartonella henselae (BH). The majority of cases of CSD are associated with exposure to cat saliva or feces, caused by a cat scratch (2–7). Chronic bacteremia typically occurs in young cats, under the age of 2 (6, 7). BH spreads from feline to feline by the cat flea (5); fleas and ticks can also transmit the infection to humans (8, 9). The most common manifestation of CSD in immunocompetent patients is regional lymphadenopathy caused by a granulomatous and suppurative reaction in the affected lymph nodes. The process eventually
A.R. Chaudhry1, M.R. Chaudhry2, J.C. Papadimitriou2, C.B. Drachenberg2 1
Department of General Surgery, Sinai Hospital of Baltimore, Baltimore, Maryland, USA, 2Department of Pathology, University of Maryland School of Medicine, Baltimore, Maryland, USA Key words: Bartonella henselae; solid organ transplant; rejection; vasculitis; cat scratch disease; post-transplant lymphoproliferative disorder; lymphadenopathy; renal biopsy; kidney transplant; skin biopsy; post-infectious complications; necrotizing glomerulonephritis; rapidly progressive glomerulonephritis; ANCA; pauci-immune glomerulonephritis Correspondence to: Arif R. Chaudhry, MD, Sinai Hospital of Baltimore, Department of General Surgery, 2401 Belvedere Ave, Baltimore, MD 21201, USA Tel: 410-601-9000 Fax: 410-601-5891 E-mail: [email protected]
Received 17 November 2014, revised 14 January 2015, accepted for publication 16 February 2015 DOI: 10.1111/tid.12376 Transpl Infect Dis 2015: 17: 411–417
resolves leaving lifelong immunity (10). Chronic exposure and low-grade infections can also lead to partial immunity (9, 11). In immunocompromised patients, most infections by the genus Bartonella are caused by B. henselae and Bartonella quintana (11). The pathogenicity of these infections varies with the subspecies involved and the host immunity, which to a large extent determines the type and severity of the clinical presentation (12, 13). In contrast with the typical self-limited CSD, Bartonella infections in immunocompromised patients may be associated with more severe and systemic symptoms
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accompanied by widespread granulomatous suppurative lesions in lymph nodes, liver, and spleen, and the formation of pseudo-neoplastic angioproliferative lesions (14). The heterogeneous clinical presentation of CSD is highlighted by multiple reports describing unusual locations for the infectious lesions, including bone (15), lungs (16), eyes (12, 17), parotid gland (18), and cardiac valves (19). Furthermore, an increasing number of putatively immune para-infectious or post-infectious disorders have been reported in association with Bartonella infections affecting the central nervous system (20– 22) and other organs (see Table 1; 8, 15–19, 21–57). Specifically, a case of post-infectious chronic active myocarditis has been reported (58), as well as renal involvement in the form of immune-complex mediated or pauci-immune acute glomerulonephritis (23–25, 40, 59). Because of the risk of developing zoonotic infections, the guidelines from the American Society of Transplantation suggest that transplant recipients should avoid acquiring pets during the first year post transplantation, and note that young cats carry the highest risk for transmission of BH infection (22). We present the case of an adult renal transplant recipient who presented with systemic manifestations
of BH infection as well as renal allograft failure and eventual graft loss because of vasculitic complications of the infection. This case exemplifies the combination of granulomatous/suppurative symptoms with the more unusual para-infectious complications that can occur with BH infections.
Case report Our patient is a 45-year-old Caucasian woman with endstage renal disease caused by complications of longstanding type 1 diabetes mellitus and hypertension, who received an extended-criteria deceased-donor kidney transplant. The early post-transplant period was complicated by delayed graft function owing to acute tubular necrosis, which resolved within 2 weeks, and later, by severe non-infectious colitis that improved with dose adjustment of mycophenolate mofetil. Maintenance immunosuppression consisted of tacrolimus (goal 5–7 ng/mL), mycophenolate mofetil 1 g/day, and prednisone (10 mg/day). Protocol renal biopsies were performed 1 week and 30 days post transplant and showed normal glomeruli with no evidence of acute rejection. Mild interstitial fibrosis and mild hypertensive donor-related vascular disease were identified in both protocol biopsies. A serum creatinine nadir of
Reported clinicopathological associations with cat scratch disease and Bartonella henselae (or Bartonella quintana) infections
Fever
Symptoms related to bacterial/tissue colonization
Parainfectious and post-infectious complications or associations
Granulomatous/suppurative disease (30–37) Lymphadenopathy1 Localized Generalized Hepatomegaly, liver abscesses, liver masses (35) Splenomegaly (35, 38, 39) Other involvement: Sternal, lung, eyes, parotid (15–18)
Renal Glomerulonephritis: Immune complex post-infectious (23), IgA nephropathy (24) ANCA-associated glomerulonephritis (25)
Vascular processes Inflammatory/suppurative: Arteritis, endocarditis (35, 40, 41) Angioproliferative: Bacillary angiomatosis and bacillary peliosis (42–46)
Neurological Encephalitis (22) syndrome (21) Guillain-Barre Transverse myelitis (21)
Rare presentations Relapse or reinfection (8, 47) ?Donor transmission (49) Absence of lymphadenopathy (49)
Vascular Leukocytoclastic vasculitis (24, 26) Other Hemophagocytic syndrome (27–29) Pancytopenia (28) Thrombotic thrombocytopenic purpura (24)
Fever is typically present and may be associated with other systemic symptoms of infection. Pertinent references are in parentheses. Lymphadenopathy in solid organ transplant recipients: localized 28% and generalized 72%. See reference section for all cases described in solid organ recipients (15–17, 19, 27–39, 42–45, 47, 48, 50–57). IgA, immunoglobulin A; ANCA, anti-neutrophil cytoplasmic antibody.
1
Table 1
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1.8 mg/dL was recorded at day 30 and renal function was stable for the following 20 months (serum creatinine 1.8–2.00 mg/dL). At the end of the second year, the patient presented with persistent fever of unclear origin and developed generalized peripheral and mesenteric lymphadenopathy and splenomegaly. An inguinal lymph node measuring 4 cm in diameter was excised, which grossly showed multiple necrotizing lesions on its cut surface. Microscopic examination demonstrated multifocal abscesses with abundant neutrophils, surrounded by palisading histiocyte aggregates with granulomatoid features (Fig. 1A). Follicular hyperplasia was also prominent in some areas, with expansion of the interfollicular areas by prominent aggregates of atypical immunoblasts, which together with the clinical presentation raised the suspicion for a post-transplant lymphoproliferative disorder (PTLD) (Fig. 1B). Serologic and histologic studies for Epstein–Barr virus were negative and a concurrent bone marrow biopsy did not show evidence of a lymphoproliferative disorder. Warthin-Starry (silver) stain in the lymph node demonstrated scattered pleomorphic rods in the necrotic areas, which, together with the multifocal abscess formation, was suggestive of Bartonella infection (Fig. 1A). Immunosuppression was decreased while awaiting the tissue polymerase chain reaction (PCR) studies for accurate bacterial identification. Within a few days, the patient developed palpable purpura in the lower extremities and serum creatinine increased to 3.5 mg/dL. A skin biopsy demonstrated leukocytoclastic vasculitis with negative immunofluorescence studies; vascular proliferative changes or organisms were not identified (Fig. 2). A kidney transplant biopsy showed no evidence of acute rejection, however, the glomeruli were abnormal owing to focal proliferative and necrotizing glomerulonephritis (Fig. 3A). The renal biopsy was repeated immediately to allow for complete evaluation of the glomerulonephritis including light microscopic, immunofluorescence, and electron microscopic evaluation. Again, a pauci-immune proliferative necrotizing glomerulonephritis was identified, with formation of glomerular crescents (Fig. 3B). All serologic studies were negative, except for perinuclear anti-neutrophil cytoplasmic antibodies (pANCA) (1:40) with no other specificity. PCR studies from the lymph node biopsy categorized the organisms as BH. The patient was treated for 7 days with azithromycin with significant improvement of symptoms; fevers disappeared and the lymph nodes decreased in size. An inguinal lymph node biopsy after treatment demonstrated hyalinosis of the lymphoid
A
B
Fig. 1. (A) Hematoxylin and eosin (H&E) stained section of the enlarged lymph node demonstrated scattered necrotizing granulomas. Arrows mark an area of necrosis with abundant neutrophilic karyorrhectic debris embedded in granulomatoid inflammation composed of epitheliod histiocytes with abundant eosinophilic cytoplasm. Insert: Warthin-Starry stain demonstrates occasional bacillary organisms (arrows). Polymerase chain reaction studies further classified these as Bartonella henselae. (B) H&E stain of other sections of the enlarged lymph node with prominent follicular hyperplasia and expanded interfollicular areas containing an atypical immunoblastic population (insert, upper right).
structures with no evidence of infection or features consistent with a lymphoproliferative process. Renal graft function continued to deteriorate, however, and the patient returned to dialysis within 4 weeks. Kidney allograft nephrectomy was performed 2 months after the initial diagnosis of crescentic glomerulonephritis, and demonstrated end-stage kidney disease with diffuse glomerular obliteration and multiple residual glomerular crescents. Superimposed acute T-cell-mediated allograft rejection was also noted.
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Fig. 2. Hematoxylin and eosion stained skin biopsy of the purpuric lesions demonstrated leukocytoclastic vasculitis (arrows) with expansive associated dermal hemorrhage secondary to vascular rupture.
Fig. 3. Hematoxylin and eosin-stained sections of the first (A) and the third (B) renal biopsies show focal proliferative and necrotizing glomerulonephritis and diffuse crescentic/early sclerosing glomerulonephritis, respectively. Progressive increase in parenchymal scarring eventually leading to end-stage renal disease was noted from the first biopsy to the last renal sample.
The patient was clinically well and was subsequently re-listed for kidney transplantation. At the time of the first lymph node biopsy, the patient was asked about exposure to domestic animals and she indicated having 1 adult cat and a kitten at home, but did not recall being scratched by them.
Discussion Fever and generalized lymphadenopathy in an immunocompromised patient can present a diagnostic
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dilemma, with the main differential diagnosis being PTLD. In our patient who also presented with splenomegaly, a possible diagnosis of PTLD delayed the correct diagnosis of CSD. Atypical lymphoid proliferation has been described in association with CSD, which further complicates the differential diagnosis between these 2 processes (60). A comprehensive literature search identified 37 reported cases of solid organ transplant recipients who developed Bartonella infections with clinical pictures ranging from typical granulomatous suppurative lymphoid involvement to unusual presentations such as chorioretinitis (15–17, 19, 27–39, 42–45, 47, 48, 50–57). In the analysis of 29 cases by Psarros et al. (35), the majority of cases occurred in kidney transplant recipients, with only a fourth of the cases occurring in liver transplant recipients. Two-thirds of transplant patients had disseminated infection upon diagnosis. Liver transplant recipients were more prone to develop disease earlier and had more severe clinical presentations in this study (35). Additional cases involving heart and lung transplant recipients have also been reported (33, 57). Because of the potentially complex clinical presentation, the diagnosis of Bartonella infections is typically difficult and often delayed (18). The spectrum of clinical findings associated with Bartonella infections is presented in Table 1. Bacterial tissue invasion/ colonization leads to the most typical findings, including both the granulomatous suppurative lesions and the pseudoneoplastic vascular proliferations. Vascular proliferative lesions can be caused by BH and B. quintana and can involve the skin, mucosa, or other organs (28). Visceral involvement is more often seen in the liver in the form of bacillary peliosis (42). Immune complex mediated or pauci-immune postinfectious complications of Bartonella infections are also listed in Table 1. Of particular interest, in relationship to our patient, are the previously reported cases of leukocytoclastic vasculitis, which in one case preceded the lymphoglandular suppurative symptoms (24, 26). With respect to renal involvement in association with BH infections, the most common pattern is that of diffuse proliferative post-infectious glomerulonephritis secondary to immune complex deposition, typically associated with native-valve endocarditis (35, 40, 61). In our patient, similar to 2 cases previously described in native kidneys (25, 59), the glomerular findings were those of pauci-immune necrotizing crescentic glomerulonephritis of the type often associated with ANCA vasculitis. The development of ANCA antibodies after infectious processes, including Bartonella infections, is well recognized (19, 62). Subsequent antibiotic treatment
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in our case led to resolution of the granulomatous/ suppurative aspect of the infection; however, progression of the pauci-immune glomerulonephritis led to ultimate graft loss. Treatment of CSD and Bartonella infections vary significantly according to the clinical presentation. Whereas treatment appears not to be necessary in most immunocompetent patients with CSD, antibiotic therapy is essential in immunosuppressed patients with any form of Bartonella infection (63). Our patient had prompt resolution of the suppurative lymphadenopathy after initiation of antibiotic treatment; however, it is possible to speculate that delay in the beginning of antibiotic treatment contributed to the development of the post-infectious vasculitic complications that eventually led to graft loss. Aside from addition of antibiotic therapy, there are no specific guidelines for the treatment of glomerulonephritis associated with bartonellosis; steroids have been successfully used in some patients (23). Hemophagocytic lymphohistiocytosis is a systemic and potentially lethal complication specifically described in transplant recipients with BH infections (27–29). The diagnosis of Bartonella infections is based on the identification of bacteria in the affected tissues by electron microscopy or with the Warthin-Starry histochemical stain; however, both these methods are cumbersome and not specific. Detection of Bartonella species DNA in tissue samples by PCR is remarkably superior, because it is both sensitive and specific (28, 35). Bacterial cultures and serological studies are not adequate to rule out the infection (28). In summary, we present the case of a patient who was successfully treated for CSD, but eventually lost the renal allograft owing to complications of the BH infection. This case highlights the multiple aspects of Bartonella infections that can lead to difficult clinical scenarios.
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Bartonella henselae infection-associated vasculitis and crescentic glomerulonephritis leading to renal allograft loss A.R. Chaudhry, M.R. Chaudhry, J.C. Papadimitriou, C.B. Drachenberg. Bartonella henselae infection-associated vasculitis and crescentic glomerulonephritis leading to renal allograft loss. Transpl Infect Dis 2015: 17: 411–417. All rights reserved Abstract: Bartonella henselae (BH) is the main cause of cat scratch disease (CSD), which more typically presents as a self-limited localized suppurative lymphadenopathy in immunocompetent individuals. In contrast, immunocompromised patients commonly have systemic disease with life-threatening complications. In addition to the angioproliferative lesions, such as bacillary angiomatosis, an increasing number of immune post-infectious complications are being recognized with BH infections, including glomerulonephritis, vasculitis, hemophagocytic syndrome, and neurological problems. We report the case of a renal transplant recipient who developed CSD in the second year post transplantation. In addition to prolonged fever and generalized lymphadenopathy and splenomegaly requiring differentiation from a post-transplant lymphoproliferative disorder, the course was complicated by the development of dermal leukocytoclastic vasculitis and pauci-immune necrotizing and crescentic glomerulonephritis, which led to failure of the renal graft. Glomerulonephritis as a complication of CSD has never been described in a kidney allograft, to our knowledge. Awareness of the diverse clinical symptoms associated with BH, including granulomatous/suppurative lesions and other less common complications can lead to more rapid and accurate diagnosis. Also, as recommended by the current guidelines, a thorough history of pet ownership should be part of the clinical evaluation before and after transplantation for all transplant recipients.
First described by Debr e in 1950 (1), cat scratch disease (CSD) is the most common clinical syndrome related to Bartonella henselae (BH). The majority of cases of CSD are associated with exposure to cat saliva or feces, caused by a cat scratch (2–7). Chronic bacteremia typically occurs in young cats, under the age of 2 (6, 7). BH spreads from feline to feline by the cat flea (5); fleas and ticks can also transmit the infection to humans (8, 9). The most common manifestation of CSD in immunocompetent patients is regional lymphadenopathy caused by a granulomatous and suppurative reaction in the affected lymph nodes. The process eventually
A.R. Chaudhry1, M.R. Chaudhry2, J.C. Papadimitriou2, C.B. Drachenberg2 1
Department of General Surgery, Sinai Hospital of Baltimore, Baltimore, Maryland, USA, 2Department of Pathology, University of Maryland School of Medicine, Baltimore, Maryland, USA Key words: Bartonella henselae; solid organ transplant; rejection; vasculitis; cat scratch disease; post-transplant lymphoproliferative disorder; lymphadenopathy; renal biopsy; kidney transplant; skin biopsy; post-infectious complications; necrotizing glomerulonephritis; rapidly progressive glomerulonephritis; ANCA; pauci-immune glomerulonephritis Correspondence to: Arif R. Chaudhry, MD, Sinai Hospital of Baltimore, Department of General Surgery, 2401 Belvedere Ave, Baltimore, MD 21201, USA Tel: 410-601-9000 Fax: 410-601-5891 E-mail: [email protected]
Received 17 November 2014, revised 14 January 2015, accepted for publication 16 February 2015 DOI: 10.1111/tid.12376 Transpl Infect Dis 2015: 17: 411–417
resolves leaving lifelong immunity (10). Chronic exposure and low-grade infections can also lead to partial immunity (9, 11). In immunocompromised patients, most infections by the genus Bartonella are caused by B. henselae and Bartonella quintana (11). The pathogenicity of these infections varies with the subspecies involved and the host immunity, which to a large extent determines the type and severity of the clinical presentation (12, 13). In contrast with the typical self-limited CSD, Bartonella infections in immunocompromised patients may be associated with more severe and systemic symptoms
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accompanied by widespread granulomatous suppurative lesions in lymph nodes, liver, and spleen, and the formation of pseudo-neoplastic angioproliferative lesions (14). The heterogeneous clinical presentation of CSD is highlighted by multiple reports describing unusual locations for the infectious lesions, including bone (15), lungs (16), eyes (12, 17), parotid gland (18), and cardiac valves (19). Furthermore, an increasing number of putatively immune para-infectious or post-infectious disorders have been reported in association with Bartonella infections affecting the central nervous system (20– 22) and other organs (see Table 1; 8, 15–19, 21–57). Specifically, a case of post-infectious chronic active myocarditis has been reported (58), as well as renal involvement in the form of immune-complex mediated or pauci-immune acute glomerulonephritis (23–25, 40, 59). Because of the risk of developing zoonotic infections, the guidelines from the American Society of Transplantation suggest that transplant recipients should avoid acquiring pets during the first year post transplantation, and note that young cats carry the highest risk for transmission of BH infection (22). We present the case of an adult renal transplant recipient who presented with systemic manifestations
of BH infection as well as renal allograft failure and eventual graft loss because of vasculitic complications of the infection. This case exemplifies the combination of granulomatous/suppurative symptoms with the more unusual para-infectious complications that can occur with BH infections.
Case report Our patient is a 45-year-old Caucasian woman with endstage renal disease caused by complications of longstanding type 1 diabetes mellitus and hypertension, who received an extended-criteria deceased-donor kidney transplant. The early post-transplant period was complicated by delayed graft function owing to acute tubular necrosis, which resolved within 2 weeks, and later, by severe non-infectious colitis that improved with dose adjustment of mycophenolate mofetil. Maintenance immunosuppression consisted of tacrolimus (goal 5–7 ng/mL), mycophenolate mofetil 1 g/day, and prednisone (10 mg/day). Protocol renal biopsies were performed 1 week and 30 days post transplant and showed normal glomeruli with no evidence of acute rejection. Mild interstitial fibrosis and mild hypertensive donor-related vascular disease were identified in both protocol biopsies. A serum creatinine nadir of
Reported clinicopathological associations with cat scratch disease and Bartonella henselae (or Bartonella quintana) infections
Fever
Symptoms related to bacterial/tissue colonization
Parainfectious and post-infectious complications or associations
Granulomatous/suppurative disease (30–37) Lymphadenopathy1 Localized Generalized Hepatomegaly, liver abscesses, liver masses (35) Splenomegaly (35, 38, 39) Other involvement: Sternal, lung, eyes, parotid (15–18)
Renal Glomerulonephritis: Immune complex post-infectious (23), IgA nephropathy (24) ANCA-associated glomerulonephritis (25)
Vascular processes Inflammatory/suppurative: Arteritis, endocarditis (35, 40, 41) Angioproliferative: Bacillary angiomatosis and bacillary peliosis (42–46)
Neurological Encephalitis (22) syndrome (21) Guillain-Barre Transverse myelitis (21)
Rare presentations Relapse or reinfection (8, 47) ?Donor transmission (49) Absence of lymphadenopathy (49)
Vascular Leukocytoclastic vasculitis (24, 26) Other Hemophagocytic syndrome (27–29) Pancytopenia (28) Thrombotic thrombocytopenic purpura (24)
Fever is typically present and may be associated with other systemic symptoms of infection. Pertinent references are in parentheses. Lymphadenopathy in solid organ transplant recipients: localized 28% and generalized 72%. See reference section for all cases described in solid organ recipients (15–17, 19, 27–39, 42–45, 47, 48, 50–57). IgA, immunoglobulin A; ANCA, anti-neutrophil cytoplasmic antibody.
1
Table 1
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1.8 mg/dL was recorded at day 30 and renal function was stable for the following 20 months (serum creatinine 1.8–2.00 mg/dL). At the end of the second year, the patient presented with persistent fever of unclear origin and developed generalized peripheral and mesenteric lymphadenopathy and splenomegaly. An inguinal lymph node measuring 4 cm in diameter was excised, which grossly showed multiple necrotizing lesions on its cut surface. Microscopic examination demonstrated multifocal abscesses with abundant neutrophils, surrounded by palisading histiocyte aggregates with granulomatoid features (Fig. 1A). Follicular hyperplasia was also prominent in some areas, with expansion of the interfollicular areas by prominent aggregates of atypical immunoblasts, which together with the clinical presentation raised the suspicion for a post-transplant lymphoproliferative disorder (PTLD) (Fig. 1B). Serologic and histologic studies for Epstein–Barr virus were negative and a concurrent bone marrow biopsy did not show evidence of a lymphoproliferative disorder. Warthin-Starry (silver) stain in the lymph node demonstrated scattered pleomorphic rods in the necrotic areas, which, together with the multifocal abscess formation, was suggestive of Bartonella infection (Fig. 1A). Immunosuppression was decreased while awaiting the tissue polymerase chain reaction (PCR) studies for accurate bacterial identification. Within a few days, the patient developed palpable purpura in the lower extremities and serum creatinine increased to 3.5 mg/dL. A skin biopsy demonstrated leukocytoclastic vasculitis with negative immunofluorescence studies; vascular proliferative changes or organisms were not identified (Fig. 2). A kidney transplant biopsy showed no evidence of acute rejection, however, the glomeruli were abnormal owing to focal proliferative and necrotizing glomerulonephritis (Fig. 3A). The renal biopsy was repeated immediately to allow for complete evaluation of the glomerulonephritis including light microscopic, immunofluorescence, and electron microscopic evaluation. Again, a pauci-immune proliferative necrotizing glomerulonephritis was identified, with formation of glomerular crescents (Fig. 3B). All serologic studies were negative, except for perinuclear anti-neutrophil cytoplasmic antibodies (pANCA) (1:40) with no other specificity. PCR studies from the lymph node biopsy categorized the organisms as BH. The patient was treated for 7 days with azithromycin with significant improvement of symptoms; fevers disappeared and the lymph nodes decreased in size. An inguinal lymph node biopsy after treatment demonstrated hyalinosis of the lymphoid
A
B
Fig. 1. (A) Hematoxylin and eosin (H&E) stained section of the enlarged lymph node demonstrated scattered necrotizing granulomas. Arrows mark an area of necrosis with abundant neutrophilic karyorrhectic debris embedded in granulomatoid inflammation composed of epitheliod histiocytes with abundant eosinophilic cytoplasm. Insert: Warthin-Starry stain demonstrates occasional bacillary organisms (arrows). Polymerase chain reaction studies further classified these as Bartonella henselae. (B) H&E stain of other sections of the enlarged lymph node with prominent follicular hyperplasia and expanded interfollicular areas containing an atypical immunoblastic population (insert, upper right).
structures with no evidence of infection or features consistent with a lymphoproliferative process. Renal graft function continued to deteriorate, however, and the patient returned to dialysis within 4 weeks. Kidney allograft nephrectomy was performed 2 months after the initial diagnosis of crescentic glomerulonephritis, and demonstrated end-stage kidney disease with diffuse glomerular obliteration and multiple residual glomerular crescents. Superimposed acute T-cell-mediated allograft rejection was also noted.
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Fig. 2. Hematoxylin and eosion stained skin biopsy of the purpuric lesions demonstrated leukocytoclastic vasculitis (arrows) with expansive associated dermal hemorrhage secondary to vascular rupture.
Fig. 3. Hematoxylin and eosin-stained sections of the first (A) and the third (B) renal biopsies show focal proliferative and necrotizing glomerulonephritis and diffuse crescentic/early sclerosing glomerulonephritis, respectively. Progressive increase in parenchymal scarring eventually leading to end-stage renal disease was noted from the first biopsy to the last renal sample.
The patient was clinically well and was subsequently re-listed for kidney transplantation. At the time of the first lymph node biopsy, the patient was asked about exposure to domestic animals and she indicated having 1 adult cat and a kitten at home, but did not recall being scratched by them.
Discussion Fever and generalized lymphadenopathy in an immunocompromised patient can present a diagnostic
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dilemma, with the main differential diagnosis being PTLD. In our patient who also presented with splenomegaly, a possible diagnosis of PTLD delayed the correct diagnosis of CSD. Atypical lymphoid proliferation has been described in association with CSD, which further complicates the differential diagnosis between these 2 processes (60). A comprehensive literature search identified 37 reported cases of solid organ transplant recipients who developed Bartonella infections with clinical pictures ranging from typical granulomatous suppurative lymphoid involvement to unusual presentations such as chorioretinitis (15–17, 19, 27–39, 42–45, 47, 48, 50–57). In the analysis of 29 cases by Psarros et al. (35), the majority of cases occurred in kidney transplant recipients, with only a fourth of the cases occurring in liver transplant recipients. Two-thirds of transplant patients had disseminated infection upon diagnosis. Liver transplant recipients were more prone to develop disease earlier and had more severe clinical presentations in this study (35). Additional cases involving heart and lung transplant recipients have also been reported (33, 57). Because of the potentially complex clinical presentation, the diagnosis of Bartonella infections is typically difficult and often delayed (18). The spectrum of clinical findings associated with Bartonella infections is presented in Table 1. Bacterial tissue invasion/ colonization leads to the most typical findings, including both the granulomatous suppurative lesions and the pseudoneoplastic vascular proliferations. Vascular proliferative lesions can be caused by BH and B. quintana and can involve the skin, mucosa, or other organs (28). Visceral involvement is more often seen in the liver in the form of bacillary peliosis (42). Immune complex mediated or pauci-immune postinfectious complications of Bartonella infections are also listed in Table 1. Of particular interest, in relationship to our patient, are the previously reported cases of leukocytoclastic vasculitis, which in one case preceded the lymphoglandular suppurative symptoms (24, 26). With respect to renal involvement in association with BH infections, the most common pattern is that of diffuse proliferative post-infectious glomerulonephritis secondary to immune complex deposition, typically associated with native-valve endocarditis (35, 40, 61). In our patient, similar to 2 cases previously described in native kidneys (25, 59), the glomerular findings were those of pauci-immune necrotizing crescentic glomerulonephritis of the type often associated with ANCA vasculitis. The development of ANCA antibodies after infectious processes, including Bartonella infections, is well recognized (19, 62). Subsequent antibiotic treatment
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in our case led to resolution of the granulomatous/ suppurative aspect of the infection; however, progression of the pauci-immune glomerulonephritis led to ultimate graft loss. Treatment of CSD and Bartonella infections vary significantly according to the clinical presentation. Whereas treatment appears not to be necessary in most immunocompetent patients with CSD, antibiotic therapy is essential in immunosuppressed patients with any form of Bartonella infection (63). Our patient had prompt resolution of the suppurative lymphadenopathy after initiation of antibiotic treatment; however, it is possible to speculate that delay in the beginning of antibiotic treatment contributed to the development of the post-infectious vasculitic complications that eventually led to graft loss. Aside from addition of antibiotic therapy, there are no specific guidelines for the treatment of glomerulonephritis associated with bartonellosis; steroids have been successfully used in some patients (23). Hemophagocytic lymphohistiocytosis is a systemic and potentially lethal complication specifically described in transplant recipients with BH infections (27–29). The diagnosis of Bartonella infections is based on the identification of bacteria in the affected tissues by electron microscopy or with the Warthin-Starry histochemical stain; however, both these methods are cumbersome and not specific. Detection of Bartonella species DNA in tissue samples by PCR is remarkably superior, because it is both sensitive and specific (28, 35). Bacterial cultures and serological studies are not adequate to rule out the infection (28). In summary, we present the case of a patient who was successfully treated for CSD, but eventually lost the renal allograft owing to complications of the BH infection. This case highlights the multiple aspects of Bartonella infections that can lead to difficult clinical scenarios.
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