Pneumonic plague, northern India, 2002.

To the Editor: A small outbreak of primary pneumonic plague took place in the Shimla District of Himachal Pradesh State in northern India during February 2002. Sixteen cases of plague were reported with a case-fatality rate of 25% (4/16). The infection was confirmed to the molecular level with PCR and gene sequencing (1). A previous outbreak in this region during 1983 was suggestive of pneumonic plague (22 cases, 17 deaths) but was not confirmed. In India, the last laboratory-confirmed case of plague was reported in 1966 from Karuataka State (2).

The index patient for the 2002 outbreak lived in a hamlet in the Himalayas. He went hunting on January 28, 2002, in a nearby forest at a height of [approximately equal to] 500-600 m from his house. There, he killed a sick wild cat and skinned it. He returned home on February 2 and sought treatment for fever, chills, and headache. On February 4, breathlessness, chest pain, and hemoptysis developed; radiologic findings were suggestive of lobar pneumonia, and treatment with augmentin was begun. He died the next day. Subsequently, 13 of his relatives exhibited a similar illness, although 2 additional patients acquired infection in the hospital. The incubation period for those patients was 1-4 days, which is consistent with that of pneumonic plague.

A team of microbiologists, epidemiologists, and entomologists visited the village after 7 more cases were reported until February 12, 2002, followed by a team from the National Institute of Communicable Diseases (NICD), New Delhi. The following case-patient definition was used: a person who sought treatment for fever of rapid onset, chills, chest pain, breathlessness, headache, prostration, and hemoptysis. A total of 16 cases were reported from 3 hospitals in the area: a local civil hospital, the state medical college, and a regional tertiary care hospital. Clinical material collected from the case-patients and their contacts was initially processed in the laboratories of these hospitals. Wayson staining provided immediate presumptive diagnosis, and confirmatory tests were performed at NICD. Diagnosis of plague was confirmed for 10 (63%) of 16 patients (1).

NICD conducted the following laboratory tests on 2 suspected culture isolates, 2 sputum specimens, 1 lung autopsy material specimen, and 1 lung lavage sample (Table): 1) direct fluorescent antibody test for Yersinia pestis; 2) culture and bacteriophage lysis test; and 3) PCR and gene sequencing to detect Y. pestis-specific genes (pla and F1). All these tests confirmed that isolates were Y. pestis and met all the World Health Organization's recommended criteria (2).

Antibodies against F1 antigen of Y. pestis were detected by passive hemagglutination testing of paired serum samples. Although 5 patients showed a >4-fold rise, 1 patient showed a >4-fold fall in antibody titer. In contrast, samples from 6 patients were negative for Y. pestis, and no change was found in the titers from 1 patient. No serum sample was collected from the index patient; for the 2 other patients who died, 1 of the single serum samples became contaminated, and the other was positive for Y. pestis (3). Paired serum samples from the case-patients were collected on a single day 4 weeks apart during the visit of the NICD team, regardless of the duration of symptoms.

Antimicrobial drug sensitivity testing was carried out by the Kirby-Bauer disk diffusion method. All isolates were sensitive to doxycycline, tetracycline, chloramphenicol, streptomycin, ciprofloxacin, gentamicin, and amikacin but were resistant to penicillin.

No fleas or other ectoparasites were found on the 6 cats, 8 dogs, 6 cows, 4 calves or 2 trapped rodents in the village. One serum sample, with pooled blood from 3 dogs was negative for antibodies against F1 antigen. Before these infections occurred, a heavy snowfall in the region had reduced the activity of rodents and was unfavorable for the survival and multiplication of rat fleas. The snow also helped restrict the spread of the infection because of reduced movement of the local population (1).

Primary pneumonic plague is acquired by inhaling infective droplets from persons or animals and rarely by accidental aerosol exposure. Y. pestis is a category A agent of bioterrorism (4). It is not truly airborne; person-to-person transmission requires face-to-face exposure within 2 m of a coughing patient (2). During 1977-1998, in the western United States, 23 cases of cat-associated human plague were reported. Bites, scratches, or other contact with infectious material while handling infected cats resulted in 17 cases of bubonic plague, 1 case of primary septicemic plague, and 5 cases of primary pneumonic plague (5).

In our report, close and prolonged contact with the index patient while providing care (for example, wiping his face during hemoptysis, supporting him during a bout of coughing, taking him to the hospital in a vehicle) resulted in secondary cases. Because of the severe winter, poor ventilation in houses further helped the illness spread. All patients acquired infection before plague was suspected. Initially, patients were treated for community-acquired pneumonia, which delayed the proper treatment and led to deaths. A patient admitted for status epilepticus was infected by her attendant, who in turn, acquired infection from a terminally ill plague patient for whom he provided some care. The patient with epilepsy and her attendant shared a common room with the terminally ill wife of the index patient, which was small and poorly ventilated. Surprisingly, the relative of the index case-patient who had accompanied him to the forest survived the infection; whereas, the wife and sister of the index patient died. No spread to healthcare workers was noted.

When plague was suspected immediate preventive measures were taken, for example, fumigation of the index patient's residence and any vehicles used for transporting the patients; active surveillance and education; standard work precautions; chemoprophylaxis for patient contacts and paramedics; and isolation and treatment of patients (1). The transmission rate for primary pneumonic plague is relatively low compared with that of many other communicable diseases; the average number of secondary cases per primary case is 1.3, according to a study done by Gani and Leach (6).

The key element in the control of small outbreaks of primary pneumonic plague could be the intensity of disease surveillance system (6). As a result, the state government has established a Plague Surveillance Unit in District Shimla of Himachal Pradesh in 2002 (1).

Acknowledgments

We thank B.D. Negi for his selfless service in collecting and processing samples from patients and their contacts in harsh field conditions. We are also thankful to NICD, New Delhi, for confirming Y. pestis in the culture isolates and serum samples.

Manohar Lal Gupta * and Anuradha Sharma *

* Indira Gandhi Medical College, Shimla, Himachal Pradesh, India

References

(1.) Outbreak of pneumonic plague in village Hatkoti, District Shimla, Himachal Pradesh, India, February 2002. New Delhi (India): Directorate General of Health Services, Ministry of Health and Family Welfare; April 30, 2002.

(2.) Dennis DT, Gage KL, Gratz N, Poland ID, Tikhomirov E. Plague manual: epidemiology, distribution, surveillance and control. Geneva: World Health Organization; (WHO/CDS/CSR/EDC/99.2); 1999.

(3.) Investigation report on "acute febrile illness with haemoptysis" outbreak in Hatkoti village, Jubbal-Kotkhai block of Shimla District, Himachal Pradesh, February 2002. New Delhi (India): National Institute of Communicable Diseases; 2002

(4.) Dennis DT, Chow CC. Plague. Pediatr Infect Dis J. 2004;23:69-71.

(5.) Gage KL, Dennis DT, Orloski KA, Ettestad P, Brown TL, Reynolds PJ, et al. Cases of cat-associated human plague in the Western US, 1977-1998. Clin Infect Dis. 2000;30:893-900.

(6.) Gani R, Leach S. Epidemiologic determinants for modeling pneumonic plague outbreaks. Emerg Infect Dis. 2004;10:608-14.

Address for correspondence: Anuradha Sharma, Mohindera Apartments, Nav-Bahar, Shimla, 171002, (H.P.), India; email: [e-mail]

Table. Epidemiologic characteristics and laboratory findings of
patients with suspected cases of pneumonic plague, India, 2002 (1) *

Patient    Relation to index      Age,    Onset of
no.             patient          y/sex    symptoms        Outcome

1            Index patient        35/M     Feb 2        Died Feb 5
2                 Wife            29/F     Feb 6        Died Feb 14
3               Brother           26/M     Feb 7     Discharged Mar 8
4                Sister           31/F     Feb 9        Died Feb 18
5                Sister           27/F     Feb 12    Discharged Feb 25
6            Brother-in-law       35/M     Feb 12    Discharged Mar 8
7            Brother-in-law       35/M     Feb 10    Discharged Feb 21
8            Sister-in-law        38/F     Feb 9     Discharged Feb 25
9             Companion on        36/M     Feb 10    Discharged Feb 28
              hunting trip
10           Sister-in-law        37/F     Feb 12    Discharged Mar 11
11        Relative of sister-     40/F     Feb 12       Died Feb 14
                 in-law
12                Aunt            57/F     Feb 10    Discharged Mar 4
13              Neighbor          46/F     Feb 11    Discharged Feb 27
14          Son of neighbor       22/M     Feb 8     Discharged Feb 27
15              Patient           47/F     Feb 11    Discharged Feb 18
           hospitalized with
                epilepsy
16           Husband/atten-       60/M     Feb 11    Discharged Mar 11
           dant of patient 15

Patient    Wayson      Blood      Sputum     Molecular     Serologic
no.       staining      c/s         c/s       results       results

1            --         --          --          --            --
2            --         --          --       Confirmed   Single sample
                                                           positive
3            --      Yersinia       --       Confirmed     Negative
                      pestis
4            --      Y. pestis      --       Confirmed        --
5            --         --          --          --         Negative
6            --         --          --          --         Negative
7            --         --          --          --         Negative
8            --         --          --          --       >4-fold rise
9            --         --          --          --       Same titer in
                                                         paired serum
                                                           specimens
10           --         --          --          --       >4-fold rise
11        Positive   Y. pestis   Y. pestis   Confirmed     Negative
12        Positive   Negative    Y. pestis   Negative    >4-fold rise
13           --         --          --          --       >4-fold rise
14           --         --          --          --       >4-fold fall
15           --         --          --          --         Negative
16        Positive   Y. pestis   Y. pestis      --       >4-fold rise

* c/s, culture/sensitivity, --, sample not submitted, paired serum
samples were tested 4 weeks apart.