- Bacillary angiomatosis
- Bacillary angiomatosis cause
- Bacillary angiomatosis transmission
- Bacillary angiomatosis signs and symptoms
- Bacillary angiomatosis complications
- Bacillary angiomatosis diagnosis
- Bacillary angiomatosis differential diagnosis
- Bacillary angiomatosis treatment
- Bacillary angiomatosis prognosis
Bacillary angiomatosis also known as epithelioid angiomatosis is a rare skin and internal organs infection caused by intracellular Gram-negative Bartonella quintana and Bartonella henselae bacteria that primarily occurs in immunocompromised persons and HIV-positive patients 1), 2), 3), 4), 5), 6), 7), 8), 9), 10), 11), 12). More recent case reports had brought into attention the probability that Bacillary angiomatosis may manifest in otherwise healthy individuals, triggered by trauma and skin burns 13). Cats are the most important reservoir for Bartonella henselae bacteria and the transmission between cats is through a flea vector (Ctenocephalides felis) 14). In healthy individuals, the infection with Bartonella bacterium can lead to the ‘cat scratch disease’ 15). In these situations, almost 90% of patients admit a recent contact with a cat (a scratch or a bite) 16). Although bacillary angiomatosis is treatable and curable, it may be life threatening if untreated.
Bartonella quintana bacterium has a human reservoir and among humans it can be transmitted by body lice (Pediculus humanus) and fleas as well, especially in the context of poverty, lack of hygienic conditions and homelessness 17), 18). Furthermore, Bartonella quintana bacterium was the causative organism of trench fever among militaries in World War 1 19).
In both immunodeficient and healthy patients, Bartonella henselae can produce bacillary angiomatosis, but in this case, fleas may play a major role in transmitting the infection to humans, considering the fact that only 20% of patients or less admit exposure to cats 20), 21). In order to sustain this hypothesis, Bartonella henselae DNA was detected in fleas 22), 23), 24).
Bacillary angiomatosis usually manifests as skin angioma-like tumor masses (vascular malformations or angiomas) or internal organs infection 25). Bacillary angiomatosis is the second-most-common cause of angiomatous skin lesions in persons infected with the human immunodeficiency virus (HIV). Multiple lesions often demonstrate more than 1 morphologic appearance. Black patients, in particular, may bear the plaque form. Bacillary angiomatosis lesions may be solitary or multiple and spreading to internal organs can occur. Bone lesions and subcutaneous masses are associated with Bartonella quintana, whereas hepatic peliosis (peliosis hepatis) and lymph node lesions are associated with Bartonella henselae 26).
Histologic examination of the lesions from the affected organs shows vascular proliferation with characteristic lobes, several mitoses with cell atypia, and leukocyte infiltration. In the majority of cases, the diagnosis is confirmed by histopathology with Warthin-Starry staining, which shows clamps of bacteria in the involved tissues, although the polymerase chain reaction test can be helpful. In differential diagnosis, the Kaposi sarcoma and pyogenic granuloma must be considered first 27), 28).
The drug of choice in the treatment of bacillary angiomatosis is erythromycin or doxycycline antibiotic. To avoid relapses, at least a 3-month therapy is recommended 29). For patients with multisystem bacillary angiomatosis involvement, a combination therapy with rifampicin can be helpful; however, interactions between the selected drugs must be carefully considered, especially in transplant recipients treated with tacrolimus 30). For such patients, the treatment with tacrolimus requires dose adjustment based on its blood concentration 31), 32).
Figure 1. Bacillary angiomatosis
Footnotes: Bacillary angiomatosis clinical appearance. Angiomatous papule and nodules (a) arm and (b) fingers. A 26-year-old healthy woman had developed papules and nodules on the right arm 6 months ago. Despite treatment with short course systemic antibiotics the lesions had enlarged and gradually extended to the forearm and hand and also to her fingers.[Source 33) ]
Figure 2. Bacillary angiomatosis
Footnote: Bacillary angiomatosis tumor-like skin lesions in a solid organ transplant recipient[Source 34) ]
Figure 3. Bacillary angiomatosis skin lesions
Footnote: A 65-year-old man reported to the dermatology department with fever and numerous nodular skin lesions 5 months after kidney transplant. (A and B) The physical examination demonstrated multiple painless blood-red papules and nodules from 5 to 15 mm in diameter, localized on the arms, trunk, thighs, and face. Some papules and nodules were covered with a fine, tightly adherent scale. Oral and genital mucosa was free of lesions. The patient complained of high fever with chills and muscle pain in the evening.[Source 35) ]
Figure 4. Bacillary angiomatosis histology
Footnote: Bacillary angiomatosis histology on skin biopsy. (C) Nodule under epidermis built of proliferating small blood vessels (hematoxylin and eosin stain). (D) High-power view of Warthin-Starry stain demostrating small extracellular aggregates of coccobacilli (arrowheads) confirming the diagnosis of bacillary angiomatosis.[Source 36) ]
Who gets bacillary angiomatosis?
Bacillary angiomatosis is seen predominantly with drug-induced immunosuppression, particularly organ transplant recipients, chronic lymphocytic leukemia, and those with HIV/AIDS. However, otherwise healthy individuals, including children, can also contract bacillary angiomatosis infection such as after major local trauma and skin burns 37). Cats are the most important reservoir for Bartonella henselae bacteria and the transmission between cats is through a flea vector (Ctenocephalides felis) 38).
Bacillary angiomatosis cause
Bacillary angiomatosis is caused by Bartonella quintana and Bartonella henselae, gram-negative intracellular bacteria. While both Bartonella species cause skin lesions, subcutaneous and bone lesions are more frequent with Bartonella quintana, and Bartonella henselae causes peliosis of the liver and spleen 39). Cats are the main reservoir for Bartonella henselae and humans for Bartonella quintana 40). Although bacillary angiomatosis infection may be spread via cat bites and scratches, fleas and body lice are the major route of transmission 41), 42), 43), 44), 45), 46). Bartonella quintana is transmitted by the human body louse (Pediculus humanus) and fleas.
In addition to bacillary angiomatosis, Bartonella henselae and Bartonella quintana cause a variety of other diseases, including endocarditis, cat scratch fever, trench fever, and peliosis hepatis 47), 48), 49), 50), 51), 52).
Once Bartonella bacteria are inoculated by blood-sucking arthropods or penetrate the skin after exposure to cat, the gram-negative bacteria attach themselves to a variety of host cells, which include red blood cells (erythrocytes), monocytes, macrophages, and dendritic cells. The endothelial cell is an important target for Bartonella quintana but not so much for Bartonella henselae.
There are several mechanisms employed by Bartonella species to enter the host cells and are the result of complex interactions at the cell surface between the bacterial and host cell proteins. Therefore, Bartonella species are highly host-specific. First, adhesion of the bacteria to the host cell membrane is followed by uptake of groups of Bartonella in a vacuole by the host cell. In a second mechanism, bacteria accumulate on the host cell surface and induce self-phagocytosis. This process results in phagosome where Bartonella species must survive the harsh environment resisting enzymes of oxidative stress. Both are well-equipped to deal with intracellular oxidative stress and produce heat shock proteins. A third mechanism is specific for entry into the erythrocytes, which involves secretion of a protein called deformin. Deformin causes, invaginations of the erythrocyte membrane providing entry points for these bacteria which are adept at rearranging the cell cytoskeleton once they are attached to the cell surface. These bacteria are the carpenters of the bacterial world 53).
The pathogenesis of bacillary angiomatosis is a proliferation of vascular endothelial cells stimulated by the angiogenic factor, what leads to the development of skin lesions, mostly described as violaceus papules, nodules, and plaques 54), 55)..
Bartonella is the only genus known to release factors that stimulate endothelial cells to produce angiopoietin-2 and epidermal production of vascular endothelial growth factor 56). The physiopathology of the blood vessel proliferative process in bacillary angiomatosis is based on the production of angiogenetic molecules, such as vascular endothelial growth factor (VEGF) and interlukin-8 (IL-8) 57), 58), 59). BadA protein on the cell surface of Bartonella henselae is responsible for adhesion to endothelial cells and fibronectin 60). BadA protein is responsible for promoting angiogenesis in Bartonella henselae infections. BadA protein is also known to promote angiogenesis via inducible hypoxia factor-1 (IHF-1). Expression of outer membrane proteins (Vomp) is responsible for promoting vascular growth in the case of B. quintana.
The ability to enter the erythrocytes protects these Bartonella species from the host’s adaptive and innate immune response. The CD4 T-helper cells produce interferon gamma and TNF alpha, which are responsible for eliminating Bartonella bacteria. The Bartonella species are capable of attenuating the host immune response thereby establishing a chronic asymptomatic carrier state. An asymptomatic carrier state caused by Bartonella quintana exemplifies this in homeless patients 61).
Bacillary angiomatosis risk factors
Risk factors for bacillary angiomatosis include the following:
- HIV infection 62), 63)
- Chronic lymphocytic leukemia
- Cytotoxic chemotherapy
- Organ transplantations 64), 65), 66).
Additional risk factors for bacillary angiomatosis associated with Bartonella henselae infection include the following:
- Cat ownership
- Cat bites
- Cat scratches
Additional risk factors for bacillary angiomatosis associated with Bartonella quintana infection include the following:
- Low socioeconomic status
- Exposure to body and hair lice
Bacillary angiomatosis was reported in a patient who was HIV-seronegative but had idiopathic thrombocytopenic purpura (ITP), had undergone splenectomy, and had been administered long-term systemic prednisone 67).
Another report described an immunocompetent child with infected facial wound, in the vicinity of which bacillary angiomatosis lesions had developed. Similar lesions also appeared at the donor site of the skin graft, which was grafted on the facial wound 68). A case of bacillary angiomatosis presenting as a pyogenic granuloma of the hand in an otherwise apparently healthy man recently was reported from Saudi Arabia 69).
Multiple leg ulcers caused by bacillary angiomatosis without a history of direct contact with cats in healthy adult man has also been reported 70).
A case of bacillary angiomatosis in an HIV-negative patient who had chronic hepatitis B but no other immunosuppressive status was reported from Turkey, suggesting that immunologic differences secondary to chronic hepatitis B could have led to an increased risk for the disease 71). Bacillary angiomatosis may be triggered by trauma and skin burns immunocompetent individuals 72), 73).
Bacillary angiomatosis transmission
In nature, cats are the reservoir of Bartonella henselae. Cats may have episodes of asymptomatic bacteremia where the bacteria have adapted to life within the red blood cells (erythrocytes) 74). Bartonella infection is acquired by cats via cat fleas (Ctenocephalides felis) when they carry Bartonella henselae or Bartonella quintana 75). Transmission of Bartonella bacteria to humans by cats occur when cats scratch humans. The human body louse Pediculus humanus transmits Bartonella quintana to humans.
Transmission to humans via cat fleas has been hypothesized but not documented 76). Transmission to humans via ticks has been reported. Bartonella henselae has been isolated from both cat scratch disease and lesions in bacillary angiomatosis.
Humans are considered the only reservoir for Bartonella quintana. However, Japanese macaques (Macaca fuscata or snow monkey) have recently been found to be another reservoir of Bartonella quintana. Bartonella quintana has been implicated in bacillary angiomatosis but has never been associated with cat scratch disease. Body louse transmits Bartonella quintana in homeless, low socioeconomic and impoverished populations 77).
The specific Bartonella species, Bartonella henselae or Bartonella quintana, can affect the location of bacillary angiomatosis, as follows:
- Skin lesions: Result almost equally from Bartonella henselae and Bartonella quintana infections
- Subcutaneous lesions: Usually caused by Bartonella quintana infection
- Bone lesions: Usually caused by Bartonella quintana infection
- Visceral involvement: Almost exclusively caused by Bartonella henselae infection
- Neurologic disorders: Associated more frequently with Bartonella quintana infection than with Bartonella henselae
Domestic cats (Felis domesticus) are the reservoirs of B henselae, which may be transmitted via cat bites or scratches or, potentially, by bites from cat fleas (Ctenocephalides felis). Kittens are more frequently associated with transmission of B henselae than are older cats. Humans appear to be the only reservoir of B quintana; the human body louse, Pediculus humanus, is the transmission vector.
Bacillary angiomatosis signs and symptoms
Bacillary angiomatosis skin lesions are usually the first sign of bacillary angiomatosis infection 78):
- Papules and nodules, range in size from pinpoint to 10 cm
- Purple, violaceous, or bright red in color
- Single lesion or many hundreds
- Any skin or mucosal site can be involved, although rarely the palms and soles
- In HIV, large subcutaneous tumors may form
- Lesions may bleed easily
- Overlying skin surface may become ulcerated or crusted
The typical bacillary angiomatosis skin lesions appear as single or multiple bright red to deep purple dome-shaped papules, nodules, or plaques 79), 80). As the number of skin lesions increase, the patient may develop high fever, tender swollen lymph nodes, nausea, vomiting, night sweats, chills, muscle aches and pain (myalgias), weakness and poor appetite 81), 82).
Bacillary angiomatosis can affect almost any organ system, although most commonly it affects skin and subcutaneous tissue. Subcutaneous lesions may erode into underlying bones (ie, osseous bacillary angiomatosis), especially the tibia, fibula, and radius. Involvement of ribs and vertebrae has been described. Rarely, skeletal muscles may be involved, resulting in pyomyositis. Mucous membranes of the conjunctiva, upper airway, and perineum (anus and penis) may also be affected. Bacillary angiomatosis may be accompanied by disseminated visceral disease (peliosis), mainly in the liver (peliosis hepatis), spleen, and lymph nodes.
Other internal organs that may be involved by bacillary angiomatosis include the following 83), 84), 85):
- Bone marrow
- Lymph noded
- Adrenal glands
- Uterine cervix
- Vulva 86)
Angioproliferative lesions of the liver and spleen are called bacillary peliosis 87).
Extrinsic compression of the common bile duct by enlarged peripancreatic, celiac, and portohepatic nodes has been reported.
Bacillary angiomatosis is often clinically indistinguishable from Kaposi’s sarcoma, which similarly presents as red to purple papules, nodules, or plaques in immunocompromised patients. Differentiating bacillary angiomatosis from Kaposi’s sarcoma is largely reliant on skin biopsy with histopathologic examination, which, for bacillary angiomatosis, demonstrates protuberant endothelial cells surrounded by clumps of bacilli that are visible with Warthin-Starry staining 88).
Bacillary angiomatosis complications
Bacillary angiomatosis may affect the heart, brain, liver, spleen, larynx, lymph nodes and gastrointestinal tract. Complications include gastrointestinal bleeding, encephalopathy, endocarditis, laryngeal obstruction and disfigurement due to the extensive lesions 89), 90).
Bacillary angiomatosis diagnosis
Bacillary angiomatosis should be suspected clinically, particularly in an immunocompromised patient.
Skin biopsy is the preferred method of diagnosing bacillary angiomatosis 91). Skin biopsy shows lobular blood vessel proliferation with epithelioid endothelial cells, and an inflammatory infiltrate including neutrophils. The microorganisms can be seen as basophilic clumps in the stroma and confirmed on Giemsa or Warthin-Starry stain (Figure 4).
In routine clinical practice, histological methods are used to confirm the diagnose bacillary angiomatosis. The hematoxylin and eosin (H and E) stain demonstrate endothelial-lined peliosis spaces. Warthin-Starry stain shows clumps of bacteria. The histological methods cannot make a diagnosis to the species level.
Differentiating bacillary angiomatosis histologically from other benign and malignant vascular proliferations, including Kaposi’s sarcoma, is facilitated by the use of histochemical (ie, Warthin-Starry staining to detect Bartonella bacilli) and immunohistochemical (ie, anti- HHV-8) stains.
Culture and serology are insensitive 92), 93).
Although polymerase chain reaction (PCR) is sensitive, specific and can be used to identify the causative agent, it is expensive and is used primarily for research or in the rare clinical setting when no skin lesion is present to biopsy 94), 95).
In resource-limited settings, where Warthin-Starry and immunohistochemical stains may not be available, distinguishing between bacillary angiomatosis and Kaposi’s sarcoma can be challenging, as the pathologist must rely on routine histopathologic poorly clues 96). Both bacillary angiomatosis and Kaposi’s sarcoma may have nodular architecture on low power and are composed of thin-walled vessels. Bacillary angiomatosis lesions have well-developed capillaries and inflamed stroma that harbors clumps of basophilic bacilli and acute inflammatory cells. On the other hand, Kaposi’s sarcoma is composed of ill-developed vasculature with slit-like spaces, prominent spindle cells, many extravasated erythrocytes, and siderophages. These features are less commonly seen in bacillary angiomatosis. Additionally, Kaposi’s sarcoma often has an abundance of plasma cells, in contrast to the mixed infiltrate, including neutrophils, that serve as an additional clue to the diagnosis of bacillary angiomatosis.
Bacillary angiomatosis histology
Histologically, the lesions of bacillary angiomatosis closely resemble pyogenic granuloma. Typically, there are ulcerated papules or nodules composed of lobules of highly vascularized edematous connective tissue (Figure 4). There is typically a mixed-cell infiltrate and nuclear dust of degenerated inflammatory cells. Accompanying this peculiar background are diagnostic clumps of pink-purplish granular material (Figure 4C). This granular material consist of huge numbers of the gram-negative rods of Bartonella henselae (Figure 4D).
Bacillary angiomatosis differential diagnosis
The clinical differential diagnosis for bacillary angiomatosis skin lesions may include Kaposi’s sarcoma, Carrion disease, pyogenic granuloma, cherry angioma, dermatofibroma, hemangioma, mycobacterial infection such as tuberculosis, coccidioidomycosis, cryptococcosis, and histoplasmosis 97).
Bacillary angiomatosis treatment
Bacillary angiomatosis is treated with antibiotic. The antibiotic of choice is macrolide erythromycin (Erythromycin 500mg four times daily) or doxycycline (Doxycycline 100mg twice daily) 98), 99). In patients who are not able to tolerate erythromycin or doxycycline, azithromycin or clarithromycin may be used 100). Mild bacillary angiomatosis skin lesions can be treated for 12 weeks 101). The response is seen by three to four weeks 102). The nodule size and the number may be followed to determine the response to the antibiotic therapy. If the response is not satisfactory, the duration of the antibiotic therapy can be extended 103). Antibiotic therapy can cure most bacillary angiomatosis skin lesions. Even peliosis responds to antibiotic therapy 104). The duration of antibiotic therapy has not been determined and most likely longer in cases with invasive systemic disease. Antibiotics should be continued for 3-6 months to prevent recurrence 105). Infectious disease consultations should be obtained. Sometimes a surgical consultation may be required for adjunctive procedures like cryotherapy, electrodesiccation with curettage, and surgical excision of solitary cutaneous lesions.
For patients with multisystem bacillary angiomatosis involvement, a combination therapy with rifampicin can be helpful; however, interactions between the selected drugs must be carefully considered, especially in transplant recipients treated with tacrolimus 106). For such patients, the treatment with tacrolimus requires dose adjustment based on its blood concentration 107), 108).
In patients who are immunosuppressed, therapy should be continued till the CD4 T-helper cell count normalizes. In HIV patients, antiretroviral therapy is essential however a case of immune reconstitution inflammatory syndrome has been reported 109). Therapy in HIV patients should be continued until the CD4 count remains above 200 cells/microliter for over six months 110).
Large pus-filled lymph nodes or blisters may need to be drained. Supportive therapy includes hydration and analgesics for pain and fever. Warm moist compresses to affected lymph nodes may decrease swelling and tenderness 111).
Bacillary angiomatosis prognosis
Bacillary angiomatosis resolves rapidly when antibiotic therapy is instituted early, antibiotics are curative in most patients 112). Skin lesions of bacillary angiomatosis disappear with days to weeks of starting appropriate treatment, although response can be incomplete. Hyperpigmentation or slight induration at the site of a lesion may persist indefinitely.
Relapses are common in immunocompromised patients and can occur after cessation of antibiotic therapy. However, if systemic bacillary angiomatosis infection is not treated promptly it can be fatal 113).
Overall bacillary angiomatosis prognosis depends on early detection and treatment and on the degree of immunosuppression. Treatment may be more difficult and requires a longer duration of therapy if the diagnosis is delayed. Untreated bacillary angiomatosis may be progressive and life threatening 114).
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