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Table 1 Included studies of human psittacosis outbreaks and the laboratory testing methods used for Chlamydia psittaci

From: Laboratory methods for case finding in human psittacosis outbreaks: a systematic review

Article, publication year[reference] Outbreak year, country Population, setting Laboratory test C. psittaci, numbers positive/numbers tested Remarks
  PCR Serology (name test, numbers) Culture  
Huminer et al., 1988 [31] 1986–1987, Israel 8 Families in contact with pet birds or domestic fowl No IPA 24/36 with 8/36 seroconversion IgM Throat swab 22/35 8 Family outbreaks with exclusion of C. pneumoniae by MIF; 1 case possible person-to-person transmission; 3 outbreaks with sick household birds (parrots) as index case.
Bourke et al., 1989 [27] NM, UK Family with aviary outside house No CFT 3/9 and MIF 3/9 Nasopharyngeal aspirates, after antibiotics 0/3(?) Serological cross-reactions with C. trachomatis and C. pneumoniae gave difficulties.
CDC, 1990 [11] 1989, USA Workers turkey processing plant No CFT 40/60 BAL specimen, 1 (seropositive) case 24/40 Hospitalized.
Samra et al., 1991 [32] 1987, Israel Family owning 3 parrots of which 2 recently died No IPA (IgM, IgG, IgA,) 4/4 Saliva, throat, sputum 3/4 2/4 Patients developed hepatitis.
Morrison et al., 1991 [39] 1989, UK Employees and visitors pet shop, after delivery new Agapornis birds No CFT 7/7 No 2 Patients died.
CDC, 1992 [26] 1992, USA 2 Families bought pet birds (parakeet, cockatiel) linked to bird distributor No CFT family A 1/1, family B 2/6 No Child and mother of family A mucopurulent conjunctivitis.
Hedberg et al., 1989 [12] 1986, USA Workers at turkey farm and processing plants No CFT 122/697 workers; 122/186 suspected cases No 13 Hospitalized.
Hinton et al., 1993 [13] 1989–1990, Australia Workers duck farm and processing plant No CFT 19/25 with 3/19 seroconversion or IgM positive No 3 Symptomatic cases; Significant association length of employment and presence of antibodies; Isolation of C. psittaci in birds.
Schlossberg et al., 1993 [21] 1991–1992, USA Contacts private aviary in basement and outdoors with poultry, psittacine birds, canaries and finches No CFT 13/24 (1 confirmed, 10 presumptive, 2 suspected cases) No Joint swelling 3 cases, 1 case had a rash and 3 seropositive cases without symptoms.
Davies et al., 1995 [28] NM, UK Cases associated with 2 linked aviaries(e.g. parrots, cockatiels, parakeets) No CFT 9/12, IF or CFT positives 9/9 No Bird contact reported by 5/9 cases. 1 Fatal case. IF to exclude C. pneumoniae.
Hughes et al., 1997 [42] 1994, USA Hospital staff and roommate exposed to pet-shop worker with psittacosis No MIF IgM, IgG 5/8 ? Person-to-person transmission likely; Cross-reactivity possible as 3 cases were also MIF seropositive for C. pneumoniae.
Goupil et al., 1998 [14] 1990, France Workers poultry slaughterhouse, truck driver, maintenance mechanic No CFT or IF seroconversion with 5 week interval 18/56 No Retrospective study symptomatic workers of whom 6 pneumonia and 4 hospitalized.
Moroney et al., 1998 [22] 1995, USA Owners of recently bought birds originating from 1 breeder (parakeets, finches, cockatiels, love birds, conures, canaries, parrots) No MIF 10/58 No Human outbreak identified after diagnosis of chlamydiosis in birds. Clinical illness did not correspond with serological response.
Williams et al., 1998 [23] 1995, Australia People living close to forest with many native parrots Post-mortem lung tissue 1/1 IF screening 16 positive; CFT 14/16 (four-fold rise or seroconversion) No Case-control study; < 2% seropositivity among controls; 1 person died possibly infected by person-to-person transmission. Comment in [59, 60].
Lederer et al., 1999 [15] NM, Germany Comparison of (a) 82 workers chicken, duck, and geese processing plant of whom 8 symptomatic with; (b) 83 workers other chicken processing plant and (c) 82 non-occupationally exposed No (a) CFT/IPA 57/82 and MIF 13/25 (b) CFT/IPA 16/83 and MIF 0/8; (c) CFT/IPA 22/82 and MIF 0/17 No 10/18 Workers employed < 3 months had serological signs of recent infection. Two cases died of multi-organ failure, 6 others had pneumonia. Also tested for C. pneumoniae and C. trachomatis in MIF.
Ito et al., 2002 [41] NM, Japan Family, index case visited confectionary with parakeets No CFT and MIF 2/2 ? Possible person-to-person transmission between sisters. Index case rising CFT titer, sister static high CFT titer. C. pneumoniae and C. trachomatis checked by MIF.
Telfer et al., 2005 [24] 2002, Australia Residents with direct or indirect wild bird contact (parrots, doves, currawongs, magpies) (Only for exclusion C. pneumoniae 0/8) MIF 59/95 with 35/59 seroconversion or 4-fold titer rise; 33/35 also 4-fold rise CFT; 3 MIF negatives had 4-fold rise in CFT No Case-control study. 2 ICU cases. Probable source wild birds in yards; 1 king parrot tested C. psittaci positive. MIF/EIA for exclusion C. trachomatis and MIF C. pneumoniae. No evidence of infection by other respiratory pathogens in probable C. psittaci cases.
Saito et al., 2005 [40] NM, Japan Owner and co-worker of pet shop selling parrots, parakeets and budgerigars No CFT 2/2; MIF 2/2 (seroconversion) ? Cross-reactivity with ELISA for C. pneumoniae. Infection by Chlamydophilia avium in a couple working in a pet shop. Comment about nomenclature Chlamydophilia avium [61]
Heddema et al., 2006 [20] 2004, Netherlands Students and staff veterinary teaching hospital in contact with cockatiels, Amazon parrots and pigeons OmpA RT-PCR 6/29 (sputum, throat swabs) R-ELISA 9/29, CFT on r-ELISA positive sera 6/9 No 3 Hospitalized cases including 1 ICU. Not all PCR positives also seropositive or vice versa. Genotype of C. psittaci PCR positive parrots matched with human cases.
Kaibu et al., 2006 [30] 2005, Japan Family; index patient bought cockatiel parakeet from pet shop Pharyngeal swab, 0/2 MIF four-fold rise 4/4 Pharyngeal swab 0/2 Dead bird C. psittaci PCR positive. C. pneumoniae and C. trachomatis also tested by MIF.
Harkinezhad et al., 2007 [46] NM, Belgium Veterinarian and veterinary assistant, tested after visiting parrot relief/breeding center, and manager of this center OmpA nested PCR 3/3, genotype-spec RT-PCR 2/3 pharyngeal, nasal swabs ELISA 2/2 Pharyngeal, nasal swabs 2/3 First report of transmission of genotype E/B from African grey parrots to humans. Veterinarian and assistant had only mild or no clinical signs.
Tiong et al., 2007 [16] 2003–2004, Australia Workers duck abattoir and farm with ducks in open sheds in contact with wild birds No ELISA 53/97; IF 35/53 No 44/53 Cases reported symptoms and 5/12 pneumonia cases hospitalized. IF to exclude C. pneumoniae and other Chlamydiae spp. cross-reactions. 18/53 Significant cross-reaction to C. pneumoniae.
Berk, 2008 et al., [3] 2007, Netherlands Visitors, participants bird show with many different bird species RT-PCR 3/11 (2/11 throat swab, 1/5 sputum, 0/7 urine, 0/11 serum) CFT 0/11 initial sample but seroconversion 9/11 No 23/> 200 Visitors ill and 11 hospitalized. Many CFT positives were not PCR positive. Bird source was a Siskin (not a psittaciformes).
Branley et al., 2008 [44] 2005, Australia Staff veterinary surgery handling sick, wild psittacine bird Spp. spec PCR (genus spec PCR) throat swab 1/3 (1/3), blood 1/3 (1/3), urine 0/3 (2/3) MIF IgG 3/3 0/3 First report of PCR analyses on human blood and urine samples for diagnosing psittacosis and first report of using PCR for comparison organism load in human psittacosis patients compared to that of sick source bird. Wild bird culture positive. MIF and PCR (urine) negative for C. trachomatis (0/3).
Çiftçi et al., 2008 [29] NM, Turkey Family, bought 2 parrots a month ago No MIF 2/2 No? First report of psittacosis from Turkey.
Gaede et al., 2008 [17] 2005, Germany Veterinary officer, poultry breeders at infected poultry farm RT-PCR and DNA micro-array assay BAL 2/2 and urine 1/1 CFT 111 samples of 65 ‘contacts’ – data not clear. 7 hospitalized cases positive. All CFT positive also MIF positive No 17/24 Suspected human cases and 7 hospitalized confirmed cases, of whom 3 admitted to ICU; 1 patient died. C. pneumoniae tested by MIF. Birds PCR positive.
Matsui et al., 2008 [18] 2001–2002, Japan Staff, students and visitors of bird park with hothouses No CFT 3/3 and MIF 14/14 symptomatic cases; MIF 8/91 non-symptomatic staff members No 13/17 Hospitalized cases. Cross-reactions C. pneumoniae and C. trachomatis excluded by MIF.
Verminnen et al., 2008 [36] 2005–2006, Belgium Turkey farmer and 2 scientists at turkey farm Nested PCR 3/3 (sputum, pharyngeal, nasal swabs) MIF 0/3 r-ELISA 3/3 3/3 Environmental monitoring study, not strictly an outbreak study. In air samples, chlamydial organisms detected by nested PCR. PCR C. pneumoniae and C. trachomatis negative.
Laroucau et al., 2009 (1) [37] 2006, France Workers at duck farms and wife of worker PCR 3/4 (1 BAL, 2 tracheal aspirates, 0 throat swab) MIF 5/5 Tracheal aspirates 1/4; BAL, throat swab negative 5 Severe psittacosis cases but avian flu was suspected at first. Ducks and human cases linked by PCR sequencing OmpA gene. Cross-reactions C. pneumoniae and C. trachomatis checked by MIF.
Belchior et al., 2011 [19] 2008, France Participants bird fair organized by breeders of Psittacidae 2 RT-PCR 2/3 throat swab MIF 2/29 (probable cases) No Retrospective cohort (n = 86) study, AR 33/86, 11/48 suspected cases hospitalized, 29/48 tested by serology.
Yang et al., 2011 [38] 2009, China Peacock farmers of a flock of sick peacocks Genotyping OmpA on isolate IF IgG 4/4 20 days post infection Throat swab 1/4 First report of psittacosis in peacocks and peacock farmers.
McGuigan et al., 2012 [43] 2011–2012, Scotland (UK) Outbreak investigation after pneumonia in 4 family members and 1 health care worker RT-PCR 3/6, spp. specific PCR 3/3 CFT positive in 3 confirmed cases, 1 probable case and 4 possible cases No Person-to-person spread to healthcare worker with same PCR OmpA strain as index case and to 1 possible case staying at ICU with index case. Suspected C. pneumoniae outbreak turned out to be C. psittaci outbreak after PCR specification (spec RT-PCR C. pneumoniae 0/3).
Williams et al., 2013 [34] 2008, England (UK) Poultry (mainly ducks) processing plant production line workers, engineering staff and visiting administrator DNA microarray genotyping on DIF positive sputum sample 1/1 (Paired) CFT and WHIF; WHIF 7/9, 5/7 WHIF positive, 4/9 WHIF recent or rising CFT No 2/3 Hospitalized cases ICU. AR 4% (9/225); 16/63 Persons some evidence of C. psittaci infection, 9/63 cases met case definition, 6/9 were symptomatic and sputum of 4/9 cases tested by DIF; 4/4 DIF positive. Cases only in plant processing free-range ducks.
Wallensten et al., 2014 [25] 2013, Sweden Hospitalized psittacosis patient who transmitted the bacterium to family, hospital room mate and medical staff PCR OmpA 3/3 (BAL) MIF 4/11 IgM, 6/11 IgG, convalescent 1/6 IgM, 3/6 IgG No Human-to-human transmission proven and index ICU patient died. His wife and 5 other secondary cases needed hospitalization: 7 confirmed, 3 probable, 1 possible case; MIF negative for C. trachomatis and C. pneumonia
Laroucau et al., 2015 [35] 2013, France Women with chicken gutting activities on a mixed poultry farm RT-PCR Chlamydiaceae-spec 23SrRna specific IncA 4/5 sputum, 0/4 throat swabs MIF 2/8 No 8 Hospitalized cases; throat swabs taken after start medication, 4 confirmed, 1 probable, 3 possible cases; in chickens C. psittaci and C. gallinacea detected
De Boeck et al., 2016 [33] 2013, Belgium Belgian couple and daughter bought lovebird in pet shop in the Netherlands Nested PCR OmpA 2/2, genotyping RT-PCR, pharyngeal swab Indirect IF IgM 1/3, IgG 2/3 Pharyngeal swab 2/2 Couple hospitalized; daughter, tested after self-treatment. One patient seronegative but PCR positive. Birds and humans both genotype A
Chan et al., 2017 [45] 2014, Australia People of veterinary school and horse stud farm in contact with fetal membrane of specific mare No EIA 3/3, MIF 0/3 4-fould rise, MIF 1/3 single high titer, MIF 2/3 falling titer No 2 Hospitalized cases. AR 56%, 3 probable, 2 suspected cases of 9; mare serology EIA positive for Chlamydial spp. and fetal membrane qPCR positive; foal died 1 week old
  1. Legend Table 1
  2. BAL broncho-alveolar lavage, CFT complement fixation test, DIF direct immunofluorescence test, EIA enzyme immuno-assay, ELISA enzyme-linked immunosorbent assay, r-ELISA recombinant ELISA, ICU intensive care unit, IF immunofluorescence test, IgA/IgM/IgG immunoglobulin A/M/G, IPA indirect immunoperoxidase assay, MIF micro-immunofluorescence test, NM not mentioned, OmpA outer membrane protein, PCR polymerase chain reaction, RT real-time, spp species, spec specific, WHIF whole cell immunofluorescence test; ? data not clear