Clinical ImplicationsCampylobacter infection is an important diagnosis to consider in primary immunodeficiency patients with chronic or recurrent diarrhea, particularly in those with very low diagnostic immunoglobulin levels. Macrolides, aminoglycosides, and/or carbapenems are promising treatment options for this potentially debilitating condition. Campylobacter infection is an important diagnosis to consider in primary immunodeficiency patients with chronic or recurrent diarrhea, particularly in those with very low diagnostic immunoglobulin levels. Macrolides, aminoglycosides, and/or carbapenems are promising treatment options for this potentially debilitating condition. Campylobacter infection, usually by Campylobacter jejuni, is the most common cause of bacterial enteritis in the world. In healthy individuals, the infection is self-limiting, but in patients with immunodeficiency, recurrent or persistent symptomatic infection may occur. In this case series, we present a cohort of primary immunodeficiency patients with chronic or recurrent Campylobacter enteritis from the United Kingdom and review the previously published literature. To identify relevant cases, a request was circulated via the UK Clinical Immunology mailing list, which includes 41 centers. Primary immunodeficiency (PID) cases with confirmed Campylobacter in stool or colonic tissue, by culture or PCR, and symptoms of longer than 3-month duration or 3 or more symptomatic flares, were included. Successful clearance of the infection was defined as resolution of symptoms and no recurrence for at least 3 months. In parallel, a literature review was performed to identify previously published cases in PubMed, using the terms “chronic,” “recurrent,” “Campylobacter,” “enteritis,” “diarrhoea,” “immune deficiency,” “immunodeficiency,” and “hypogammaglobulinemia.” Six centers replied, reporting 13 cases of chronic or recurrent Campylobacter enteritis in total: 4 from Queen Elizabeth Hospital (Glasgow), 3 from Southmead Hospital (Bristol), 2 from Royal London Hospital (London), 1 from Frimley Park Hospital (Surrey), 1 from Derriford Hospital (Plymouth), 1 from Northern Care National Health Service Foundation Trust (Greater Manchester), and 1 from Gloucester Royal Hospital (Gloucester). Patients were all adults, aged 21 to 71 years, with the vast majority (n = 12) having common variable immunodeficiency (CVID, Table I). Laboratory investigations at diagnosis revealed undetectable (<0.1 g/L) serum IgA in 85% (11 of 13) of cases and IgM in 62% (8 of 13). Where data were available, very low (<1 g/L) pretreatment serum IgG was seen in 67% (6 of 9) of cases. Low circulating B cells (<0.1 × 109 cells/L), natural killer cells (<0.1 × 109 cells/L), and T cells (<0.67 × 109 cells/L) were seen in 58% (7 of 12), 33% (4 of 12), and 17% (2 of 12) of cases, respectively. In patients with normal B cells and where B-cell immunophenotyping was performed, 67% (2 of 3) had low (<2%) class-switched memory B cells (Table I).Table IUK cohort with PID and recurrent or persistent Campylobacter enteritis: Immunologic profileCaseImmune deficiencyComorbiditiesDiagnostic serum immunoglobulin levels (g/L) & postvaccination responses (where data are available)Diagnostic lymphocyte subsets (×109 cells/L)Immunoglobulin replacement (at Campylobacter diagnosis)Trough immunoglobulin level (at Campylobacter diagnosis)1CVIDBronchiectasis, proliferative bronchiolitis, asthma, obesity, raised alcohol intakeUndetectable IgA & IgMB cells 0.05, normal T & NK cellsIVIg 25 g every 3 wk8 g/L2CVIDExcised brain tumor with residual learning difficulties, previous B-cell lymphoma, pulmonary nodules, splenomegalyIgG 0.8, undetectable IgA & IgMB cells <0.01, T cells 0.15, NK cells <0.01IVIg 70 g every 2 wk13.1 g/L3CVIDIntermittent low-level CMV and EBV viremiaIgG 19 (units /mL), undetectable IgA, IgM 0.11B cells 0.02 T cells 0.14, NK cells 0.01 (class- switch memory B cells 0.9%, CD21 low B cells 6%)IVIg 30 g every 3 wk6.2 g/L4CVIDNoneUndetectable IgG, IgA, & IgM with poor response to Pneumococcal polysaccharide vaccineB cells <0.01, normal T cells, NK cells 0.03SCIg 20 g every week12.1 g/L5CVID (NFKB2 mutation)Asthma, chronic rhinosinusitisIgG 3.6, undetectable IgA, IgM 0.16 with poor response to Pneumococcal polysaccharide vaccineB cells 0.01, normal T & NK cellsIVIg 40 g every 3 wk10.9 g/L6CVIDBronchiectasis, hypersplenism, ulcerative colitisUndetectable IgA & IgMNASCIg 14 g every week11 g/L7XLA (btk mutation confirmed)BronchiectasisIgG 0.73, undetectable IgA, IgM 0.29B cells <0.01, normal T & NK cellsIVIg 40 g every 3 wk10.4 g/L8CVIDNoneIgG 0.7, undetectable IgA & IgM with poor response to Pneumococcal polysaccharide vaccineNormal B, T, & NK cells (class- switch memory B cells 1%)IVIg 35 g every 3 wk7.5 g/L9CVIDBronchiectasisIgG 3.8, IgA 0.53, IgM 0.61 with poor response to Pneumococcal polysaccharide vaccineNormal B, T, & NK cellsNo (patient declined)3.8 g/L10CVIDNoneUndetectable IgA & IgMB cells 0.03, normal T cells, NK cells 0.05IVIG 30 g every 3 wkNA11CVIDInterstitial lung disease, ischemic heart diseaseUndetectable IgG, IgM, & IgA with poor response to Pneumococcal polysaccharide vaccineNormal B, T, & NK cells (class- switch memory B cells 0.6%)No (began after Campylobacter diagnosis)<1.1 g/L12CVIDBronchiectasis, chronic sinusitisIgG 0.69, undetectable IgA & IgM with poor response to Pneumococcal polysaccharide vaccineNormal B, T, & NK cellsSCIg 12 g every week11.7 g/L13CVIDLiver nodular regenerative hyperplasia, monoclonal gammopathy of undetermined significanceIgG 3.37, IgA 0.38, IgM 0.25 with poor response to Pneumococcal polysaccharide vaccineNormal B, T, & NK cells (class-switch memory B cells 6.3%)No (patient declined)3.4 g/LCMV, Cytomegalovirus; EBV, Epstein Barr virus; IVIg, intravenous immunoglobulin; NA, not available; NK, natural killer; SCIg, subcutaneous immunoglobulin.Undetectable = <0.1 g/L for IgA & IgM, <1 g/L for IgG. Open table in a new tab CMV, Cytomegalovirus; EBV, Epstein Barr virus; IVIg, intravenous immunoglobulin; NA, not available; NK, natural killer; SCIg, subcutaneous immunoglobulin. Undetectable = <0.1 g/L for IgA & IgM, <1 g/L for IgG. The total duration of gastrointestinal symptoms varied from 10 months to 17 years, and symptoms were intermittent in 6 patients (Table II). Three patients also exhibited malabsorption and/or weight loss, and 4 had systemic symptoms and/or bacteremia. In all cases, Campylobacter jejuni was isolated, with 3 patients harboring strains that were resistant to multiple antibiotics. Detection was by stool culture in most (n = 11), but 2 patients were positive only by colonic tissue culture or PCR analysis. In certain patients, other potential causes of chronic diarrhea were detected, for example, colon inflammation, duodenal villous atrophy, and chronic norovirus infection (Table II). Clinically however, Campylobacter remained the most likely cause for their symptoms, with onset and resolution of the diarrhea coinciding with Campylobacter detection (Table II).Table IIUK cohort with PID and recurrent or persistent Campylobacter enteritis: Clinical features, microbiology, and antimicrobial therapyCaseAge at symptoms onset (y), sexGastrointestinal symptoms/ malabsorption, and durationNo. of Campylobacter- positive samplesOther GI investigationsSystemic symptomsUnsuccessful antibiotic courses (temporary or no clinical improvement)Successful antibiotic course (symptoms resolution & no recurrence for >3 mo)142, MChronic diarrhea for 10 mo10× Campylobacter jejuni (MCS stool, multiresistant)Stool: calprotectin normal; negative for other bacteria, parasites, Norovirus, Enterovirus;GI endoscopy: chronic active pancolitisNoneMultiple PO clarithromycin,IV ertapenem,IV meropenemIV 1 g once a day ertapenem for 4 wk with PO neomycin for 7 d255, MIntermittent diarrhea with malabsorption and weight loss for 8 y13× C jejuni (MCS stool, multiresistant)Stool: calprotectin >600 μg/g; Norovirus+, negative for other bacteria, parasites, Enterovirus;GI endoscopies: chronic villous atrophy in duodenum, widespread focal active colitisEpisodes of arthralgia, headache and fever but negative blood MCS for Clostridium difficilePO doxycycline, clarithromycin, azithromycin, ciprofloxacin,cotrimoxazoleIV 1 g once a day ertapenem for 4 wk with PO neomycin for 7 d353, MIntermittent diarrhea for 17 y3× C jejuni (MCS stool)Stool: Norovirus+ negative for other bacteria, parasites;GI endoscopies: antral gastritis, increased intraepithelial lymphocytes and substantial villous atrophy in duodenum, mild active chronic inflammation without granulomata in colonNone (blood MCS not tested)PO coamoxiclav, neomycin, rifaximin, immunoglobulin; IV meropenem, ertapenem(spontaneous resolution)460, MChronic diarrhea with malabsorption and weight /protein loss3× C jejuni (PCR & MCS stool, multiresistant)Stool: negative for other bacteria, parasites, Norovirus, Enterovirus, Adenovirus, Astrovirus, Rotavirus, Sapovirus;GI endoscopies: nil significantSeveral episodes of bacteremia (MCS confirmed)PO azithromycin; IV carbapenem, aminoglycoside, chloramphenicolIV meropenem & aminoglycoside, PO ciprofloxacin532, FChronic diarrhea for 2 y4× C jejuni (PCR & MCS stool)Stool: calprotectin 116 μg/g; Norovirus+, Helicobacter pylori+Negative for other bacteria, parasites, Enterovirus, Adenovirus, Astrovirus, Rotavirus, SapovirusNone (blood MCS not tested)NonePO azithromycin 500 mg once a day with ciprofloxacin 500 mg twice a day for 3 wk654, MChronic diarrhea for 10 mo3× C jejuni (2× MCS & 1× PCR stool)Stool: negative for other bacteria, parasitesNonePO erythromycin, azithromycin, coamoxiclav(ongoing infection)724, MIntermittent diarrhea for 3 y>10× C jejuni (MCS stool)Stool: H pylori+, calprotectin 500 μg/g; negative for other bacteria, parasites, Norovirus, Adenovirus, Astrovirus, Rotavirus, Sapovirus;GI endoscopy: colon cryptitis with crypt abscessesEpisode of suspected bacteremia (blood MCS not tested)PO ciprofloxacin, azithromycinIV meropenem for 10 d829, MIntermittent diarrhea for 12 y2× C jejuni (MCS stool)NoneNone (blood MCS not tested)NonePO clarithromycin926, FChronic diarrhea for 6 mo with weight loss1× C jejuni (MCS colonic tissue)Stool: calprotectin 907 μg/g; negative for other bacteria, parasites;GI endoscopy: severe inflammation in lamina propria with cryptitis, crypt abscess formation and prominent lymphoid follicles in right & transverse colon, mild chronic inflammatory infiltrate in left colon, negative CMV stainsFevers but negative blood MCS for C difficilePO ciprofloxacinPO azithromycin 500 mg once a day for 2 wk1060, MIntermittent diarrhea for 15 y with weight loss5× C jejuni (MCS stool)NoneNone (blood MCS not tested)NonePO erythromycin 500 mg 4 times a day for 2 wk1171, MIntermittent diarrhea for 8 y3× C jejuni (MCS stool)Stool: negative for other bacteria, parasites, Norovirus, Adenovirus, Astrovirus, Rotavirus, Sapovirus;GI endoscopy: normal colonNone (blood MCS not tested)PO clarithromycin 500 mg twice a day for 2 wk(patient passed away)1248, FIntermittent diarrhea for 4 y4× C jejuni (MCS stool)Stool: calprotectin >600 μg/g; negative for other bacteria, parasites, Norovirus, Adenovirus, Astrovirus, Rotavirus, SapovirusNone (blood MCS not tested)PO ciprofloxacin 500 mg twice a day for 2 wk, clarithromycin 3 d (not tolerated)PO ciprofloxacin 500 mg twice a day for 2 wk1355, FIntermittent diarrhea for 8 y2× C jejuni (MCS stool)Stool: negative for other bacteria, parasites, Norovirus, Adenovirus, Astrovirus, Rotavirus, Sapovirus;GI endoscopy: focal mild acute inflammation in cecumNone (blood MCS not tested)NonePO clarithromycin 500 mg twice a day for 1 wkF, female; GI, gastrointestinal; IV, intravenous; M, male; MCS, microscopy, culture & sensitivities, includes screen for Salmonella, Shigella, Giardia, Escherichia coli O157, Cryptosporidium, Giardia; PO, per os (by mouth); PCR, polymerase chain reaction. Open table in a new tab F, female; GI, gastrointestinal; IV, intravenous; M, male; MCS, microscopy, culture & sensitivities, includes screen for Salmonella, Shigella, Giardia, Escherichia coli O157, Cryptosporidium, Giardia; PO, per os (by mouth); PCR, polymerase chain reaction. Fifty-eight percent (7 of 12) of patients were on adequate immunoglobulin replacement (serum IgG trough ≥ 8 g/L) when they developed enteritis (Table I). In patients who successfully cleared the infection and had no relapse, oral macrolides (n = 5, azithromycin, clarithromycin, or erythromycin) and intravenous carbapenems (n = 4, meropenem or ertapenem) were most commonly used, followed by aminoglycosides (n = 3, eg, neomycin), oral ciprofloxacin (n = 3), and coamoxiclav (n = 1), either alone or in combination. A literature review identified 32 published cases of recurrent or persistent Campylobacter enteritis or multiple Campylobacter spp. stool isolation in PID (see Table E1 in this article’s Online Repository at www.jaci-inpractice.org). Most were in X-linked agammaglobulinemia (XLA, n = 17), whereas 5 were in CVID and 3 in Good syndrome. Based on their diagnosis, very low or absent circulating B cells were expected to be present in at least 69% (22 of 32) of these cases, 18 with agammaglobulinemia and 3 with Good syndrome. The total duration of symptoms varied from 3 months to 15 years and resulted in weight loss in 7 of 32 (22%) cases. Sixty-six percent (21 of 32) also developed Campylobacter bacteremia, in some cases recurrent. Most stool cultures revealed C jejuni (n = 25), with Campylobacter coli being isolated in 6 cases and 1 patient harboring both. At least 20 of 32 (63%) patients were on immunoglobulin replacement when they developed enteritis, and these cases were more likely to clear the infection (80% vs 58% those who were not). The institution of immunoglobulin therapy alone led to resolution of the infection in 3 of 32 (9%) patients.1Schønheyder H.C. Søgaard P. Frederiksen W. A survey of Campylobacter bacteremia in three Danish counties, 1989 to 1994.Scand J Infect Dis. 1995; 27: 145-148Crossref PubMed Scopus (0) Google Scholar,2Borleffs J.C.C. Schellekens J.F. Brouwer E. Rozenberg-Arska M. Use of an immunoglobulin M containing preparation for treatment of two hypogammaglobulinemic patients with persistent Campylobacter jejuni infection.Eur J Clin Microbiol Infect Dis. 1993; 12: 772-775Crossref PubMed Scopus (0) Google Scholar In those patients who successfully cleared the infection, oral macrolides were most commonly used (n = 10; erythromycin, clarithromycin, or azithromycin), followed by aminoglycosides (n = 5; neomycin, gentamicin, netilmicin, or kanamycin), carbapenems (n = 5; meropenem, biapenem, or imipenem), tetracyclines (n = 4; doxycycline or minocycline), metronidazole (n = 3), fosfomycin (n = 2), ciprofloxacin (n = 1), and piperacillin (n = 1). Antibiotics were administered for a duration of 4 or more weeks in 7 of 32 (22%) cases. Overall, recurrent or persistent Campylobacter enteritis may contribute to significant morbidity in patients with PID, including debilitating diarrhea, malabsorption, weight loss, electrolyte disturbances, and bacteremia. A high index of suspicion for Campylobacter infection should be kept in these patients, particularly in those who have previously tested positive. Campylobacter can persist in the intestinal tract only giving intermittent symptoms and reinfection is commonly by the same microorganism.3Okada H. Kitazawa T. Harada S. Itoyama S. Hatakeyama S. Ota Y. et al.Combined treatment with oral kanamycin and parenteral antibiotics for a case of persistent bacteremia and intestinal carriage with Campylobacter coli.Intern Med. 2008; 47: 1363-1366Crossref Scopus (16) Google Scholar Furthermore, Campylobacter is difficult to grow even in specific culture media, and there are no validated consensus mechanisms to measure the bioburden in the gut flora, let alone eradication.4Buss J.E. Cresse M. Doyle S. Buchan B.W. Craft D.W. Young S. Campylobacter culture fails to correctly detect Campylobacter in 30% of positive patient stool specimens compared to non-cultural methods.Eur J Clin Microbiol Infect Dis. 2019; 38: 1087Crossref Scopus (25) Google Scholar Colonic tissue culture or stool PCR may thus be necessary in patients with ongoing symptoms.4Buss J.E. Cresse M. Doyle S. Buchan B.W. Craft D.W. Young S. Campylobacter culture fails to correctly detect Campylobacter in 30% of positive patient stool specimens compared to non-cultural methods.Eur J Clin Microbiol Infect Dis. 2019; 38: 1087Crossref Scopus (25) Google Scholar Other causes of chronic diarrhea should also be considered in these patients, particularly in those who remain symptomatic despite Campylobacter eradication. Most cases in our series were patients with CVID (12 of 13), in contrast to previously published cases where XLA was the most frequent diagnosis (17 of 32). This may echo improvements in patient management, with more patients being treated with adequate immunoglobulin replacement in recent years. The fact that fewer patients were suspected to be bacteremic in our cohort compared with previously published literature (31% vs 66%) also suggests the latter. The cases described above highlight the importance of humoral immunity in the prevention of chronicity or reinfection from Campylobacter spp. Previously published case reports suggest that patients who are on immunoglobulin therapy are more likely to clear the infection and immunoglobulin therapy alone led to eradication in a few cases. Most patients in our case series also had undetectable or very low diagnostic immunoglobulin levels. It is well established that most patients with CVID and XLA lack plasma cells in the lamina propria of their small and/or large intestine and this is important because the intestinal mucosa normally harbors the largest population of antibody-secreting plasma cells in the body.5Khan F. Person H. Dekio F. Ogawa M. Ho Hen Dunkin D. et al.Crohn’s-like enteritis in X-linked agammaglobulinemia: a case series and systematic review.J Allergy Clin Immunol Pract. 2021; 9: 3466-3478Abstract Full Text Full Text PDF Scopus (0) Google Scholar Interestingly, 58% of patients in our case series also had low or absent circulating B cells. This contrasts with what is known for CVID, where only 10% to 20% are expected to have low B cells.6Selenius J.S. Martelius T. Pikkarainen S. Siitonen S. Mattila E. Pietikäinen R. et al.Unexpectedly high prevalence of common variable immunodeficiency in Finland.Front Immunol. 2017; 8: 1190Crossref PubMed Scopus (39) Google Scholar This finding was echoed by the literature review, where 69% of patients were expected to have very low or absent circulating B cells based on their diagnosis. Low circulating B cells also seem to play an important role in the predisposition to other chronic gastrointestinal infections, like norovirus.7Grammatikos A. Moghaddas F. Reeve H. Johnston S. Gompels M. Albur M. Low circulating B cells in immunocompromised individuals are linked to poorer antibody responses to vaccines and a predisposition to viral infections.J Allergy Clin Immunol Global. 2023; 2: 111-113Abstract Full Text Full Text PDF Google Scholar Finally, 42% of patients in our case series had inadequate serum immunoglobulin trough levels when diagnosed with Campylobacter enteritis. These observations suggest that patients with CVID who are not maintained on adequate immunoglobulin replacement are at a higher risk of infection. In patients with CVID and low B cells in particular, higher IgG therapeutic targets may need to be considered. HIV-infected patients can also develop chronic or recurrent Campylobacter enteritis,8Molina J.M. Casin I. Hausfater P. Giretti E. Welker Y. Decazes J.M. et al.Campylobacter infections in HIV-infected patients: clinical and bacteriological features.AIDS. 1995; 9: 881-885Crossref PubMed Google Scholar but even in these patients, humoral immunity seems to play a key role: HIV patients who fail to clear the infection have poor Campylobacter-specific antibody responses while low CD4 T-cell levels do not seem to correlate with a worse outcome.9Perlman D.M. Ampel N.M. Schifman R.B. Cohn D.L. Patton C.M. Aguirre M.L. et al.Persistent Campylobacter jejuni infections in patients infected with the human immunodeficiency virus (HIV).Ann Intern Med. 1988; 108: 540-546Crossref PubMed Google Scholar In conclusion, Campylobacter enteritis is an important diagnosis to consider in patients with PID with chronic or recurrent diarrhea, particularly in those with very low diagnostic immunoglobulin levels. Diarrhea in CVID can be highly multifaceted and other potential causes should always be considered. We thank the patients for their collaboration and participation and the respective departments of the authors for supporting this study. Table E1Previously published cases of chronic/recurrent Campylobacter enteritis or Campylobacter spp. stool isolation in PIDLead author, year of publicationAge of onset (y), sexImmune deficiencyImmunoglobulin replacementSymptomsNo. of Campylobacter+ stool samplesFailed treatments (temporary or no clinical improvement)Definitive treatment (resulting in symptom resolution)Aguilar-Company et al,E1Aguilar-Company J. Los-Arcos I. Pigrau C. Rodríguez-Pardo D. Larrosa M.N. Rodríguez-Garrido V. et al.Potential use of fosfomycin-tromethamine for treatment of recurrent campylobacter species enteritis.Antimicrob Agents Chemother. 2016; 60: 4398-4400Crossref PubMed Scopus (9) Google Scholar 201664, FCVIDIVIg every 3 wkDiarrhea and hypovolemic shock1× Campylobacter jejuni, 1× Campylobacter coliNRPO fosfomycin 3 g every 48 h for 6 wkBarker et al,E2Barker C.R. Painset A. Swift C. Jenkins C. Godbole G. 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