Review Rheumatological Patients Undergoing Immunosuppressive

Review

Rheumatological patients undergoing immunosuppressive treatments and parasitic diseases: a review of the literature of clinical cases and perspectives to screen and follow-up active and latent chronic infections S. Fabiani and F. Bruschi

Department of Translational Research ABSTRACT Conclusions. Considering parasitic in- and New Technologies in Medicine and Objective. Nowadays, several po- fections as emerging and potentially se- Surgery, School of Infectious Diseases, tent immunosuppressive drugs are rious in their evolution, additional strat- Università di Pisa, Pisa, Italy available for patients with rheumato- egies for the prevention, careful screen- Silvia Fabiani, MD logic disorders. In general, these treat- ing and follow-up, with a high level of Fabrizio Bruschi, MD ments are acceptably well tolerated. suspicion, identification, and pre-emp- Please address correspondence to: Nevertheless, in patients with rheu- tive therapy are necessary in candidate Fabrizio Bruschi, matic diseases, who are taking immu- patients for biological agents. Scuola Medica, Via Roma 55, nosuppressive drugs, an increased risk 56126 Pisa, Italy. of bacterial, viral and fungal, as well Introduction E-mail: [email protected] as parasitic infections, exists. Rationale Received on October 14, 2013; accepted Methods. We have reviewed literature, Immunosuppressive drugs, other than in revised form on February 18, 2014. on PubMed library, on the topic “par- corticosteroids (CS), are used in the Clin Exp Rheumatol 2014; 32: 587-596. asitic infections in rheumatic disease treatment of various rheumatologic con- © Copyright Clinical and patients treated with immunosuppres- ditions to induce or maintain a remis- Experimental Rheumatology 2014. sive drugs, including biological thera- sion, to reduce the frequency of flare pies”. We used no language or time or relapse, and to guarantee disease Key words: rheumatic diseases, restrictions. Search was concluded on control. In particular, treatment options immunosuppressive therapies, January 15th 2014. We grouped all have been substantially improved in parasitic infections, parasitic screening parasitic events among rheumatologic, recent years thanks to the introduction flow-chart therapeutically immuosuppressed, pa- of disease-modifying anti-rheumatic tients to estimate the magnitude of this drugs (DMARDs), including drug-in- risk. Then we gave our viewpoint in the hibiting cytokines, such as, for example, perspective to screen and follow-up for TNF-alpha antagonists, and/or block- active and latent chronic parasitoses, ing cytokine receptors (i.e. tocilizumab developing an hypothetical flow-chart. (TCZ), a monoclonal antibody blocking Results. From data published in the the interleukin-6 receptor). In general, literature the real burden of parasi- these therapies seem to be acceptably toses, among patients with rheumatic well tolerated, however, taking into ac- diseases treated with immunosuppres- count the increased risk of infections, sive treatments, can not be estimated. the situation is less optimistic, especial- Nevertheless, a positive trend on pub- ly for patients treated with anti-TNF- lication number exists, probably due to alpha drugs (i.e. monoclonal antibodies, more than one reason: i) the increasing such as infliximab (IFX) and adalimum- number of patients treated, especially ab (ADA), soluble TNF-alpha recep- with more than one immunosuppres- tors, like etanercept (ETN), and others, sive treatment, including new biologi- certolizumab-pegol (CZP), golimumab cal agents; ii) the increasing number of (GLM), anakinra (ANA), and abatacept individuals who move from the north to (ABT) (1-14), probably because of the the south of the world (endemic areas inhibition of this crucial molecule that for parasitic infections) and viceversa, has a key role in the early phase of the due to globalisation, and iii) the fact host defense against bacterial, viral and that more attention is paid for notifica- parasitic infections (15-17). However, Competing interests: none declared. tion/publication of cases. even data obtained before the begin-

587 REVIEW Parasitic infection screening in immunosuppressed patients / S. Fabiani & F. Bruschi ning of the TNF-alpha blockers era, showed an incidence rate of infections in the rheumatoid arthritis (RA) population nearly twice as high as in matched non-RA controls. Indeed, the risk of infections in rheumatic diseases can be explained with a combination of actions defined by the disease itself, with its perturbations of immune functions and impairment of general health (18), and the use of older different kind of drugs, too, that in general interfere with immune system and that are yet routinely used in these patients [i.e. methotrexate (MTX); cyclophosphamide (CTX); cyclosporine (CSA); azathioprine (AZA)] (18-20). The cumulative immunosuppressive activity of rheumatologic treatments, both traditional and new drugs, Fig. 1. PRISMA flow chart: data collection and selection of studies. continues to represent one of the main factor predisposing for infections, es- exists, probably also due to the re- OR rheumatic patients AND immuno- pecially in concomitant use of CS (21), cent greater attention for notification / suppressive therapies OR biological with some variations related to the dose publication of cases, but mainly to the DMARDs OR anti-tumour necrosis and the duration of CS treatment (22). increasing number of patients treated, factor (TNF)-alpha. We used no lan- Thus, despite different mechanisms of especially with more than one immu- guage or time restrictions. The search action, and the lack of strict correlation nosuppressive treatment, including was concluded on January 15th 2014. between a specific drug and a particular new biological agents, and the advance type of infection, any immunosuppres- of the era of globalisation with more Results sive therapy can facilitate any type of and more people having contact with Study selection infection (23-27). In particular, many endemic areas for certain diseases, the We identified and screened 45 records. bacterial (28-44), viral (32, 45-49), and parasitic risk seems to be emerging in From these records we extrapolated 83 fungal (50-57) infections have been such a population. cases of interest assessed for eligibil- described among these patients. In ad- To limit the spread of this infective ity. Among these we excluded only six dition, the impact of the parasitic dis- complication in rheumatological pa- cases with concomitant manifestation eases among rheumatic disease patients tients candidate for immunosuppres- of systemic rheumatic disorders and during immunosuppressive treatments, sive agents, specific recommendations, parasitic diseases, in which no immu- including biologic therapies, is hard to based on a multidisciplinary contri- nosuppressive treatment was adminis- estimate since few reports exist in the bution and a systematic review of the tered (60, 61) (Fig. I). literature, however, recent observations literature, for screening and follow-up lead to consider parasitic infections as of active and latent chronic infections Description of results emerging in such a population (58). have to be elaborated as happened for We grouped on literature reported cas- those caused by viruses or bacteria. es of parasitic infections in rheumatic Objectives We want to give our viewpoint in the disease patients treated with immuno- With this literature review we want to perspective of a proposition to screen suppressive drugs, including biological deal with the parasitosis risk among and follow-up for parasites the patients therapies in Table I (see hereinafter). rheumatic disease patients treated with undergoing immunosuppressive treat- A positive trend, probably due to i) the immunosuppressive drugs, including ments (59). increasing number of patients treated, biological therapies. especially with more than one immu- For this purpose we analysed records Methods nosuppressive treatment, including on this topic, identified through -Pub To review case reports of parasitic in- new biological agents, ii) globalisa- Med database searching. fections on rheumatological patients tion, and finally iii) to higher attention We also grouped the clinical cases pre- in immunosuppressive treatment, and for notification/publication of cases, sented in literature to estimate if the risk analyse the magnitude of the data, we exists. First case reports of parasitoses of parasitoses among the patient catego- searched the literature on PubMed li- during anti TNF agents treatments ap- ry considered actually exists and if the brary combining the terms parasitic peared in 2003, more or less 5 years af- problem can be considered as emerging. diseases OR parasitic infections OR ter the introduction of these drugs into As a positive trend on publications parasitoses AND rheumatic diseases the clinical practice.

588 Parasitic infection screening in immunosuppressed patients / S. Fabiani & F. Bruschi REVIEW

Table I. Published reported cases of parasitic infections in rheumatic disease patients treated with immunosuppressive drugs, including biologic therapies, found on PubMed (60-104).

Parasitic diseases Country Pts (Age y/sex) Rheumatologic Immunosuppressive Treatment Reference of report Disease treatments (Agents) duration (mo) before onset of parasitic disease

Chagas disease Brazil 43/F RA CS NA Cossermelli et al., 1978 (62) NA 1 case (y/sex NA) SLE NA NA Barousse et al., 1980 (61) NA 1 case (y/sex NA) SLE NA NA Barousse et al., 1980 (61) NA 1 case (y/sex NA) SLE NA NA Barousse et al., 1980 (61) NA 1 case (y/sex NA) SLE NA NA Barousse et al., 1980 (61) NA 1 case (y/sex NA) SLE NA NA Barousse et al., 1980 (61) Brazil 33/F SLE CS, CTX NA dos Santos-Neto et al., 2003 (63) Spain 44/F SLE CS, CTX 6 Pinazo et al., 2010 (64) Bolivia 40/F SLE CS, CTX, AM, HDX NA Pinazo et al., 2013 (60) Bolivia 46/F SLE CS NA Pinazo et al., 2013 (60) Argentina 44/F SLE CS, CTX, AZA, HDX NA Pinazo et al., 2013 (60) Leishmaniosis Israel 56/M RA MTX, CS 120 Vardy et al., 1999 (65) France 66/M ANCA-associated CTX, MTX, CS 120 Zanaldi et al., 1999 (66) vasculitis Italy 35/M BD Chlorambucil, CS 36 Sirianni et al., 2001 (67) Spain 50/M RA MTX, CS 120 Baixauli et al., 2003 (68) Italy 60/M PAN CTX, CS 2 Scatena et al., 2003 (69) Spain 55/M PsA IFX 9 Romani-Costa et al., 2004 (70) Others (no details given) 300 Italy 76/M ANCA-associated CTX, CS 36 Sollima et al., 2004 (71) vasculitis France 53/F RA IFX, AZA, CS 12 Fabre et al., 2005 (72) Italy 69/F RA ADA 25 Bassetti et al., 2006 (73) MTX, CS 360 Greece 60/F RA ETN 18 Bagalas et al., 2007 (74) CSA, CS, ANA 96 France 9/F JRA CSA, MTX, CS, ANA 60 Koné-Paut et al., 2007 (75) Italy 42/M PsA Efalizumab 3 Balato et al., 2008 (76) Greece 45/M PsA IFX, MTX, CS 60 Tektonidou et al., 2008 (77) Greece 65/F RA MTX 96 Venizelos et al., 2008 (78) Spain 56/F RA ADA 26 Balta-Cruz et al., 2009 (79) Italy 63/M PsA IFX 24 De Leonardis et al., 2009 (80) USA 42/F RA ADA 2-3 Franklin et al., 2009 (81) Spain 55/M RA IFX, MTX, CS 11 Garcia-Vidal et al., 2009 (82) France 7/F JIA ETN 11 Jeziorski et al., 2009 (83) IFX 12 Germany 31/M AS IFX 48 Mueller et al., 2009 (84) France 51/F AS ADA 20 Schneider et al., 2009 (85) Greece 55/M AS IFX, MTX 12 Xynos et al., 2009 (86) Greece 71/F GCA IFX, CS 24 MTX 12 France 50/M AS IFX 7 Hakimi et al., 2010 (87) Greece 77/F RA IFX 6 Kritikos et al., 2010 (88) Spain 60/M RA ADA 18 Moltó et al., 2010 (89) 4 cases (y/sex NA) ADA or others anti TNF-alpha NA (no details given) Spain 72/F RA ADA 1 Moreno et al., 2010 (90) Germany 38/M RA IFX 0.5 Zanger et al.,2011 (91) Microsporidiosis Brazil 38 cases (y/sex NA) RA,AS,PsA Combination therapy (MTX NA Aikawa et al., 2011 (92) and/or AZA and/or Leflunomide and/or chloroquine and/or sulfasalazine and/or CSA) plus CS Norwegian scabies NA 1 case (y/sex NA) RA TCZ NA Baccouche et al., 2011 (93) Pentatrichomonas France* 68/M RA ADA, CS NA No Author. Rheumatology 2013 (94) hominis infection Strongyloidosis NA yNA/F SLE CS ± other drugs (no details given) NA Setoyama et al., 1997 (95) NA 33/F SLE CS NA Kothary et al., 1999 (96) NA 1 case (y/sex NA) SLE CS ± other drugs (no details given) NA Reiman et al., 2002 (97) NA 1 case (y/sex NA) SLE CS ± other drugs (no details given) 36 Lemos et al., 2003 (98) NA 69/F RA CS, MTX NA Koh et al., 2004 (99) NA 35/F SLE CS NA Arsic-Arsenijevic et al., 2005 (100) NA 1 case (y/sex NA) RA ETN NA Boatright et al., 2005 (101) NA 34/F SLE, AS CS, CTX NA Mora et al., 2006 (102) NA 37/M AS CS ± other drugs (no details given) NA Krishnamurthy et al., 2007 (103) NA 63/M RA Anti TNF-alpha (no details given), CS, MTX Turkey 68/F RA, BA MTX, CS NA Altintop et al., 2010 (104)

ADA: adalimumab; AM: acid mycophenolic; ANA: anakinra; ANCA: anti-neutrophil cytoplasmic autoantibody; AS: ankylosing spondylitis; AZA: azathioprine; BA: bronchial asthma; BD: Behçet’s disease; CS: corticosteroids; CSA: cyclosporine; CTX: Cyclophosphamide; ETN: etanercept; GCA: giant cell arteritis; HDX: hydroxychloroquine; IFX: infliximab; JIA: juvenile idiopathic arthritis; JRA: juvenile rheumatoid arthritis; MTX: methotrexate; NA: not applicable; PAN: polyarteritis nodosa; PsA: psoriatic arthritis; RA: rheumatoid arthritis; SLE: systemic lupus erythematosus; TCZ: tocilizumab *: recent travel history in Burkina Faso.

589 REVIEW Parasitic infection screening in immunosuppressed patients / S. Fabiani & F. Bruschi

From the analysis of therapeutic sched- RA (62, 60), seem to suggest a possible infections does not identify “at risk”/ ule of the rheumatic patients reviewed, role of this infection in certain category exposed asymptomatic patients and this it’s clear that combined treatments pre- of patients, such as candidates for bio- leads to the low number of reported vailed and that the concomitant, long- logical agents. cases. Another important point regards term use of different type of immuno- the difficulties to diagnose and the risk suppressive agents certainly plays a cru- Discussion for erroneous diagnosis, mainly due cial role in the development of parasitic Summary of evidence to the absence of any kind of symp- diseases, although, at this moment, the Actually, with literature reported data, toms or signs, and often to the lack of true mechanisms at the basis of the in- the parasitic complication, among rhe- awareness of parasitic diseases as po- ter-relationships remain not fully clari- matologic immunosuppressed patients, tential infective complication during fied. emerge as possible and increasing, but immunosuppressive therapies also in On the basis of published data, the the real magnitude is not adequately ap- rheumatologic patients; misdiagnosis most represented parasitic infection in preciated. can also come from certain parasitoses rheumatic disease patients treated with In summary, prospective studies, to esti- attitude to mimic rheumatologic disor- immunosuppressive drugs seems to be mate the true dimension of the problem ders. In these circumstances, symptoms/ leishmaniosis, being strongyloidosis the in clinical practice and to establish po- signs presented by the patients could be second-one (see Table) (105, 106). tential co-factors and elaborate screen- completely correlated to the rheumatic According to data that show increased ing programmes to study patients before disease if no screening for parasites is microsporidia susceptibility and rate of initiating any immunosuppressive treat- carried out (122). For example clinical dissemination in immunosuppressed pa- ment, especially for therapeutic sched- presentation of the S. stercoralis hy- tients (107-110), Aikawa et al. reported ule including biological agents, and pos- perinfection syndrome may be variable positive tests for microsporidia signifi- sibly introduce prophylaxis/pre-emptive and may mimic some features of SLE, cantly higher in all types of rheumatic therapy, are needed. including pulmonary haemorrhages or disease patients compared with the con- vasculitis (102, 123). As a consequence trol subjects, and also more frequently Limitations of these misdiagnosis of strongyloido- detection microsporidia plus positive fe- Describing reported cases published in sis, patients could receive treatment for cal leukocytes in patients than in control literature to analyse the parasitic risk RA or SLE developing a disseminated subjects (92). during immunosuppressive rheumato- parasitosis because of the immunosup- Baccouche et al. described a case of logical treatments, more than one limi- pressive therapies (124-133); in leish- Norwegian scabies in a patient with tation occurs. maniosis atypical and confusing fea- RA treated with TCZ (93), and other First of all, it is unclear whether re- tures may resemble autoimmune and authors highlight as commensal non- ported cases are primary or reactivated systemic rheumatic diseases (see SLE) pathogenetic agents, such as Pentatrich- infections. In fact, rheumatic diseases at presentation and during the course omonas (formerly Trichomonas hominis patients could already be infected with of the illness (134, 72, 135-138), and or Trichomonas intestinalis), can cause certain parasites and develop disease also amebosis can mimic rheumatologic symptomatic clinical patterns (94). only after immunosuppression status diseases, but this only constitutes a dif- Studies, analysing rheumatologic pa- due to the therapies performed for their ferential diagnosis issue; in fact these tients and comparing them with healthy primary affection. For example Strongy- kind of infections, at this moment, do people, did not find any differences for loides stercoralis infection can persist in not seem appear with greater frequency pathogenic parasites (Entamoeba his- the host for several decades, and in pa- in rheumatic disease patients treated tolytica/dispar, Dientamoeba fragilis, tients who are exposed to immunosup- with immunosuppressing agents in gen- Giardia lamblia, Cryptosporidium par- pressive therapy this status predispose eral, and biological therapy in particular vum, Cyclospora cayetanensis, Isos- to a hyperinfection syndrome, which is (139-141). pora belli, Ancylostoma duodenale, characterised by a high mortality rate Moreover, in immunosuppressed pa- Ascaris lumbricoides, and Blastocystis (119-121). tients the possibility of atypical presen- hominis), and non-pathogenic parasites In addition to this limit, as regards the tation of infectious diseases (including (Endolimax nana, Entamoeba coli, and literature on this issue and in consid- the parasitic ones) is frequent, because Entamoeba hartmanni) (92). eration of the incredible number of pa- of the immune status in general and the Although Trypanosoma cruzi, has not tients affected by rheumatic diseases specific therapies for the rheumatic dis- traditionally been considered an oppor- and treated or undergoing immunosup- orders (72, 142); in this regard, especial- tunistic agent, studies on experimen- pressive therapies and of the potentially ly TNF-alpha-blocking treatment may tal models (111, 112), many reports of “at risk” patients for primary or reacti- mask the typical symptoms of infectious reactivation in immunocompromised vated parasitic infection, the phenom- diseases, constituting an additional con- patients (mainly those with AIDS) (113- ena is certainly under-reported. More founding factor. 118) and some cases, reported in the sci- than one factor may play a role in this entific literature, of coexistence of Cha- under-reporting. First of all, the lack Perspectives gas disease and SLE (61, 63, 64, 60) or of screening programmes for parasitic The Authors’ viewpoint in the perspec-

590 Parasitic infection screening in immunosuppressed patients / S. Fabiani & F. Bruschi REVIEW tive to screen and follow-up active and After anamnesis and physical exami- active infection (152, 153). Thus, con- latent chronic parasitoses is a proposal nation, blood exam for chemistry and sidering that especially in leishmanio- for a flow-chart. As many parasitic in- full blood count should be done. Eo- sis-endemic countries, where asymp- fections are clinically silent, a detailed sinophilia might be a potential marker tomatic visceral leishmaniosis (VL) interview to rheumatic disease patients to look further in screening for some infections occur more frequently than undergoing immunosuppressive treat- parasites in asymptomatic individuals, clinically apparent VL cases, leishma- ments should be performed to assess and in particular for chronic strongy- nin skin test (LST) (Montenegro test) the presence of epidemiological (citizen loidosis (143-145), not forgetting that appears to be the only screening test ca- status, living conditions, and positive its absence does not absolutely exclude pable of detecting asymptomatic Leish- travel history) and clinical (comorbidi- a parasitic infection (146-149), also mania infections. A positive LST result ties, treatments with any type of phar- because it might be often intermittent is thought to indicate durable cell-me- macological agents, previous blood (150, 151). diated immunity after asymptomatic in- transfusions and/or stem cell or solid All patients have to give several stool fection or clinical cure of VL (154) and organ transplantation), and patient-spe- sample, too, to perform microscopic VL with unusual signs and symptoms cific (alcohol and/or drug abuse) risk examination and if necessary also co- may develop in immunocompromised factors that could act as co-factors in the proculture. patients with previous LST positivity development of infective complications. Blood samples, especially in popula- after immunosuppressive treatments. In fact, epidemiological factors, such tions from endemic areas with potential Cascio and Iaria (155) suggest LST as past residence in tropical and sub- parasites-exposure history, should also along with serologic analysis; Pizzorni tropical regions, and certain personal be screened serologically for strongy- et al. recommend serological monitor- behaviors with low levels of hygiene loidosis and leishmaniosis, in particu- ing for leishmaniosis must be carried conditions or certain not fully stand- lar. Serology in strongyloidosis appears out in individuals that live in endemic ardised methodologies to screen do- the most reliable and sensitive screen- areas during therapy with anti-TNF nors, especially those with a not clear ing procedure especially in populations monoclonal antibodies, since cytokine- history of contacts with and/or travels from Strongyloides-endemic areas. Re- induced macrophage activation and tis- to endemic regions for parasites, could garding leishmaniosis, data in favour sue granuloma formation essential to facilitate exposition to parasitic agents, of the ability of the serological analysis control infection, are inhibited during and, together with comorbidities, phar- alone to screen for leishmaniosis before the use of this medication (156). macologic agents or toxic substances, initiation of biological or immunosup- No data are present in the literature with immunosuppressive effects, could pressive treatments are lacking. Evi- regarding T. gondii, but on the basis increase the risk for the development of dence indicates that serological analy- of the risk of reactivation, serology more severe disease in case of parasitic sis can identify only symptomatic or should be performed at regular interval primary infection/reactivation. asymptomatic cases with recent and still (13). Prevention measures and re-test- ing at regular interval, too, should be indicated for negative patients for the risk of more severe primary infections during immunosuppression. Thus in “at risk” patients for epidemiological and / or clinical patient-specific factors (i.e. origin or travels in endemic countries, blood transfusions or stem cells or solid organ transplantations), it could be indicated also serology for trypanosomosis. The performance of an accurate screening “flow chart” (Fig. 2) appear even more indicated especially considering that prophylaxis and pre-emptive treatment for parasitoses mentionated before are available. Nevertheless, few data exist on the use of anti-Leishmania therapies for LST- positive or serologically positive patients (155). Instead, S. stercoralis complete eradi- Fig. 2. A hypothesis of a “flow chart” to screen and follow-up for parasites rheumatic disease patients cation before the initiation of immu- undergoing immunosuppressive treatments. nosuppressive therapy is essential in

591 REVIEW Parasitic infection screening in immunosuppressed patients / S. Fabiani & F. Bruschi patients with uncomplicated infections pecially if undergoing TNF antagonists, 6. WALLIS RS, BRODER MS, WONG JY, HAN- to ensure that hyperinfection syndrome are needed (159). SON ME, BEENHOUVER DQ: Granuloma- tous infectious diseases associated with tu- does not develop (102). In general, fall- Some National Societies such as the mor necrosis factor antagonists. Clin Infect ing eosinophilia and Strongyloides an- Italian and Spanish Societies of Rheu- Dis 2004; 38: 1261-5. tibody titers are indications of success- matology (SIR and SER) and Tropical 7. BAKLEH M, TLEYJEH I, MATTESON EL, OS- ful treatment (157). Thus, a systematic Medicine (SIMET and SEMTSI) are MON DR, BERBARI EF: Infectious complications of tumor necrosis factor-alpha antago- pre-emptive course of ivermectin (one starting to plan specific recommen- nists. 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