Table 2.
Human studies showing associations between Pneumocystis and seasonal and environmental factors.
| Region/ Study authors | Year | Location | Methods | Main findings |
|---|---|---|---|---|
| USA | ||||
| Hoover, et al [19] | 1991 | MACS cohort: Four US cities | Four centre retrospective cohort study. | Incidence of PCP greater in colder cities (Chicago & Pittsburgh) than in warmer cities (Baltimore & Los Angeles): PCP diagnoses peaked in May - June and were lowest in November - December. |
| Bacchetti [20] | 1994 | USA | Analysis of monthly trends in AIDS diagnoses among adolescents and adults reported to CDC. | Seasonal pattern of PCP, with a peak in March. More PCP in MSM/bisexual men in summer in West of USA (includes San Francisco and Los Angeles) which is drier than rest of USA at this time. |
| Navin, et al [21] | 2000 | Atlanta, Georgia | Two centre single city retrospective cohort study. | PCP associated with outdoor activities (gardening, hiking or camping). |
| Dohn, et al[22] | 2000 | Cincinnati, Ohio | Single centre cohort study. | Clustering of PCP cases by Zip code. Most cases occurred in affluent areas with more green space. No seasonal variation. |
| Morris, et al [23] | 2000 | San Francisco, California | Single centre cohort study. | Clustering of PCP cases by Zip code. Most cases occurred in more residential areas that contain parks and small yards. No seasonal variation. |
| Morris, et al [24] | 2004 | MACS cohort Four US cities | Retrospective cohort study of patients who had necropsy. PCR detection of P. jirovecii. | Rates of colonization (determined by PCR) greater in cigarette smokers. Detection rates higher in Chicago and Pittsburgh (70.4% and 61.5%) than in Baltimore and Los Angeles (42.3% and 16%). |
| Djawe, et al [6] | 2013 | San Francisco, California | Single centre cohort study. | Seasonal variation in hospitalization with PCP; peak in summer (June-August). |
| South America | ||||
| Vargas, et al [25] | 2005 | Santiago, Chile | Autopsy study, two children’s hospitals. PCR detection of P. jirovecii. | P. jirovecii DNA detected in 51.7% of immune competent infants dying in the community and in 20% dying in hospital. Seasonal variation in detection: 53% in Winter (June - August) when maximum temperature = 16–18°C. and 30% in Autumn (March - May) when maximum temperature =20–28°C. |
| Djawe, et al [26] | 2010 | Santiago, Chile | Prospective cohort study. | Seasonal variation in serum antibody titers to P. jirovecii among immune competent infants. MsgA antibody titers highest in Spring (September - November) and lowest in Autumn (March- May) MsgC titers highest in Summer (December - February) and Winter (June - August) |
| Northern Europe | ||||
| Setnes & Genner [27] | 1986 | Copenhagen, Denmark | Two hospital autopsy study. | Pneumocystis identified in 83/1762 (4.7%) of autopsies at Righospitalet and Finseninstituttet Hospitals 1979–1984. Lower detection of Pneumocystis observed in 1981 corresponded with low temperature, low vapor pressure, and low humidity. Higher rate of detection in 1982–3 corresponded with higher average temperature and vapor pressure. |
| Miller, Grant & Foley [28] | 1992 | London, UK | Single centre retrospective cohort study. | Seasonal variation in PCP: highest in June-July and September, following periods with low rainfall and temperatures <13°C. |
| Vanhems, Hirschel & Morabia [29] | 1992 | Geneva, Switzerland | Single centre retrospective cohort study. | Seasonal variation in PCP cases: highest in June - September. Seasonal variation no longer observed after introduction of PCP prophylaxis. |
| Lundgren, et al [30] | 1995 | Copenhagen, Denmark | Multicenter prospective study in Northern, Central and Southern Europe. | Incidence of PCP higher in cooler climates (Northern Europe), compared with Central or Southern Europe. |
| Delmas, et al [31] | 1995 | Paris, France | Multicenter retrospective study in eight European countries and in Amsterdam, Netherlands. | Incidence of AIDS-defining PCP higher in Germany, Switzerland, and UK (Northern/Central Europe), and lowest in Portugal and Italy (Southern Europe). |
| Del Amo, et al [32] | 1998 | London, UK | Eleven center retrospective cohort study. | PCP was presenting AIDS-defining condition in 52/313 (17%) of black Africans, compared with 52/314 (34%) of non-Africans living in London. |
| Lubis, et al [33] | 2003 | London, UK | Single centre retrospective cohort study. | Variation in monthly incidence of PCP: highest in January (16.9%) associated with low monthly rainfall (<35 mm/month). January peak more prominent in some years and not evident in other years. Other peaks in April (9.8%) and September (9.6%) not associated with rainfall. |
| Miller, et al [34] | 2007 | London, UK | Single centre retrospective cohort study. Genotyping of P. jirovecii isolates at mt LSU rRNA locus. | Association between Genotype 2 and mixed genotypes, and season/month: peaks in June - July, and May - June and September, respectively. No association between temperature, or rainfall and specific genotypes. |
| Walzer, et al [35] | 2008 | London, UK | Single centre retrospective cohort study. | Seasonal variation in presentation of PCP over a 21 year period: highest in summer (June - August; 29.8%) and lowest in winter (December - February; 21.9%). |
| Sing, et al [36] | 2009 | Munich, Germany | Single centre cohort study. | Seasonal variation in cases of PCP: peak in summer (May - August). Mean temperature (but not rainfall or wind strength) associated with incidence of PCP. |
| Schoffelen, et al [37] | 2013 | Netherlands | ATHENA national observational cohort study. | PCP occurred less frequently in patients originating from sub- Saharan Africa compared to patients of Western origin (Western Europe, New Zealand, Australia); adjusted Odds Ratio = 0.21 (0.15–0.29). |
| Southern Europe | ||||
| Varela, et al [38] | 2004 | Seville, Spain | Single centre cohort study. HIV-positive and HIV-uninfected patients with PCP. | Inverse correlation between incidence of PCP and mean ambient temperature. Highest number of cases in winter (January-March, with peak in February) when mean minimum temperature was 7–9.7°C (and average temperature was 10–16.5 °C*). No association with humidity. |
| Calderon, et al [39] | 2004 | Anadalusia, Spain | Thirty two public hospitals in southern Spain. HIV-positive and HIV-uninfected patients with PCP. | Seasonal variation in PCP: highest in winter (December - February: 30.5% of all cases), compared with spring (23.9%), summer (23.7%), and autumn (21.9%). Additional peak in May. |
| Alvaro-Meca, et al [39] | 2015 | Spain | Retrospective national study of hospitalized HIV-positive patients with PCP. | Most cases of PCP occurred in winter (December - February), fewest in summer (June - August), corresponding to lowest (10– 20 °C) and highest temperatures, respectively. |
| Australia | ||||
| Tadros, et al [40] | 2017 | Melbourne, Australia | Retrospective single center study of patients with systemic autoimmune rheumatic disease. | PCP most commonly presented in Autumn (March - May) when average temperature was 13.2–20°C; no cases occurred in Winter (June - August) when average temperature was 10– 12°C*. |
Key: MACS = Multi-center AIDS cohort study; MSM = men who have sex with men; PCP = Pneumocystis jirovecii pneumonia; CDC = Centers for Disease Control and Prevention; ATHENA = AIDS Therapy Evaluation in the Netherlands; Msg = major surface glycoprotein; PCR = polymerase chain reaction; mt LSU rRNA = mitochondrial large subunit ribosomal RNA.
*
data from World Weather Online [7].