A Systematic Review of Risk of HIV Transmission Through Biting or Spitting

Implications for Policy

FV Cresswell; J Ellis; J Hartley; CA Sabin; C Orkin; DR Churchill

HIV Medicine. 2018;19(8):532-540.

Supporting Information

Full Search Description for HIV Transmission by Human Bite and Spitting

Searches were carried out by an experienced clinical librarianonOvid MEDLINE(Epub Ahead of Print, In-Process & Other Non-Indexed Citations, Daily and 1946 to Present, and Ovid Embase 1974 to 2018 Week 02. An initial search for material on HIV transmission by human bite and spitting was run on 5 January 2018, and supplemented by one on HIV transmission in saliva, executed on 9 January 2018.

Relevant natural language and controlled vocabulary terms were selected and combined, and search strategies are reproduced below. Controlled vocabulary terms were adapted where necessary from database to database. Neither MeSH nor EMTREE offer satisfactory terms for spitting, so this element was only searched for by a natural language string, and supplemented by a second broader search which used natural language and controlled vocabulary terms for saliva. Final result sets were de-duplicated and screened for relevance by the searcher, irrelevant results being discarded.

Search strategies (HIV transmission by human bite and spitting)

MEDLINE

1 "HIV INFECTIONS"/(186469)

2 exp HIV/(98730)

3 (hiv or hiv-1* or hiv-2* or hiv1 or hiv2 or "hiv infect*").ti,ab. (301184)

4 ("human immunodeficiency virus" or "human immunedeficiency virus" or "human immuno-deficiency virus" or "human immune-deficiency virus").ti,ab. (85397)

5 ("human immun*" and "deficiency virus").ti,ab. (611)

6 ("acquired immunodeficiency syndrome" or "acquired immunedeficiency syndrome" or "acquired immuno-deficiency syndrome" or "acquired immune-deficiency syndrome").ti,ab. (22349)

7 ("acquired immun*" and "deficiency syndrom*").ti,ab. (6148)

8 ("AIDS virus" or "HIV/AIDS").ti,ab. (28631)

9 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 (358436)

10 (spit or spitting or spat or expectorat*).ti,ab. (3970)

11 9 and 10 (172)

12 BITES, HUMAN/(1104)

13 (bite or bites or bitten).ti,ab. (29655)

14 12 or 13 (30072)

15 9 and 14 (341)

16 "HIV INFECTIONS"/tm (26338)

17 "ACQUIRED IMMUNODEFICIENCY SYNDROME"/tm (10755)

18 DISEASE TRANSMISSION, INFECTIOUS/(8580)

19 ((disease or virus or viral or pathogen or infection or HIV* or AIDS) adj6 (transmission or transmit*)).ti,ab. (87110)

20 16 or 17 or 18 or 19 (114091)

21 15 and 20 (194)

22 11 or 21 (365)

EMBASE

1 "HUMAN IMMUNODEFICIENCY VIRUS INFECTION"/(243655)

2 exp "HUMAN IMMUNODEFICIENCY VIRUS"/(171585)

3 (hiv or hiv-1* or hiv-2* or hiv1 or hiv2 or "hiv infect*").ti,ab. (340306)

4 ("human immunodeficiency virus" or "human immunedeficiency virus" or "human immuno-deficiency virus" or "human immune-deficiency virus").ti,ab. (85653)

5 ("human immun*" and "deficiency virus").ti,ab. (705)

6 ("acquired immunodeficiency syndrome" or "acquired immunedeficiency syndrome" or "acquired immuno-deficiency syndrome" or "acquired immune-deficiency syndrome").ti,ab. (21770)

7 ("acquired immun*" and "deficiency syndrom*").ti,ab. (6176)

8 ("AIDS virus" or "HIV/AIDS").ti,ab. (30633)

9 1 or 2 or 3 or 4 or 5 or 6 or 7 or 8 (437613)

10 (spit or spitting or spat or expectorat*).ti,ab. (5279)

11 9 and 10 (220)

12 BITE, HUMAN/(4928)

13 (bite or bites or bitten).ti,ab. (32146)

14 12 or 13 (34604)

15 9 and 14 (514)

16 "VIRUS TRANSMISSION"/(53612)

17 ((disease or virus or viral or pathogen or infection or HIV* or AIDS) adj6 (transmission or transmit*)).ti,ab. (92571)

18 16 or 17 (125778)

19 9 and 14 and 18 (180)

20 11 or 19 (396)

HIV transmission in saliva

MEDLINE:

1 *HIV INFECTIONS/tm (10617)

2 *ACQUIRED IMMUNODEFICIENCY SYNDROME/tm (4002)

3 ((disease or virus or viral or pathogen or infection or HIV* or AIDS) adj3 (transmission or transmit*)).ti,ab. (67739)

4 1 or 2 or 3 (75477)

5 *Saliva/(21502)

6 saliva.ti. (12177)

7 5 or 6 (23776)

8 4 and 7 (227)

9 ANIMALS/not (HUMANS/and ANIMALS/) (4780516)

10 8 not 9 (169)

EMBASE

1 virus transmission/and Human immunodeficiency virus infection/(15216)

2 ((HIV* or AIDS) adj3 (transmission or transmit*)).ti,ab. (25778)

3 1 or 2 (34977)

4 saliva/(32755)

5 saliva.ti. (11850)

6 4 or 5 (36212)

7 3 and 6 (154)

8 ANIMALS/not (HUMANS/and ANIMALS/) (1321042)

9 7 not 8 (153)

1 2 3 4 5

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Acknowledgements
We would like to thank Tom Roper and his fellow clinical librarians in the Medical Education Centre at Brighton and Sussex University Hospital for their help with the database search and sourcing of articles. FVC is supported by the Wellcome Trust (210772/Z/18/Z). FVC is a fellow of Makerere-UVRI Infection and Immunity Centre of Excellence. CAS has received funding from Gilead Sciences, ViiV Healthcare and Janssen-Cilag for membership of Data Safety and Monitoring Boards and Advisory Boards and for preparation of educational materials. CO has received honoraria, travel sponsorship, advisory board fees and research grants from Jannsen, MSD, Gilead and Viiv.

Table 1. Criteria applied to determine plausibility of HIV transmission relating to incident
	Plausibility
	Low	Medium	High	Confirmed
Number of cases	3	2	1	3
Documented baseline negative HIV test	No	No	Yes or no	Yes or no
Temporal relationship	Positive HIV test a significant time after the incident	Positive HIV a significant time after incident	HIV seroconversion within 2 months of incident	HIV seroconversion within 2 months of incident
Phylogenetic analysis	Not done	Not done	Not done	Phylogenetic analysis suggestive of transmission
Other potential source of HIV infection	Other HIV risk factors prior to positive HIV test	No other HIV risk factors prior to positive HIV test	No other HIV risk factors	No other HIV risk factors

Table 2. Summary table of articles included in final data set
Authors [reference]	Year	Country	Exposure (nature of incident)	Outcome (HIV seroconversion)	Nature of injury	Number exposed	Blood in mouth of perpetrator	Perpetrator HIV viraemic*	Perpetrator on ART	Plausibility of transmission attributable to bite	Comment
Tereskerz et al. 14	1996	USA	Bite (HCW)	No	Skin intact	1	Unknown	Unknown	Unknown	NA	50 bites; 1.7% from a known HIV-positive individual; no transmission reported
Tsoukas et al. 30	1988	Canada	Bites (HCW)	No	Skin intact (n = 5), skin broken (n = 3)	8	Yes	Yes	No	NA	2.5-year follow-up
Drummond 31	1986	Unknown	Bite (during seizure)	No	Skin broken	1	Unknown	Yes	No		18-month follow-up
Shirley and Ross 32	1989	USA	Bite (community, intentional)	No	Skin intact	4	Unknown	Yes	No	NA	Good follow-up of cases
Vidmar et al. 21	1996	Slovenia	Bite (during seizure)	Yes	Skin broken (nail)	1	Yes	Yes	ZDV monotherapy	High	Blood in mouth from bitten tongue and a deep injury caused to nail bed. Baseline HIV test negative and seroconversion within 1 month
Akani et al. 28	2007	Nigeria	Bite (community, intentional)	Yes	Deep bite (lip (sutured)	1	No	Unknown	Unknown	Low	HIV test negative 1 year previously but had been sexually active in the interim. Tested HIV positive during antenatal care
Batholomew and Jones 25	2006	Trinidad	Bite (community, intentional)	Yes	Skin broken	1	Yes	Yes	No	Medium	Child tested HIV positive 4 years after being bitten by father. No baseline HIV test. No other HIV risk factors reported
CDC 22	1996	USA	Bite (community, intentional)	Yes	Multiple bites	1^†	Yes	Unknown	No	Confirmed	HIV negative at time of bite and confirmed linkage on phylogenetics
Deshpande et al. 23	2011	India	Bite (community, intentional)	Yes	Deep bite (nail bed exposed)	1	No	17 163 copies/mL (plasma); 2405 copies/mL (saliva)	No	Confirmed	High-risk injury. 91% sequence homology on phylogentic analysis
Wahn et al. 26	1986	Germany	Bite (community, intentional)	Yes	Skin intact	1	No	Yes	No	Medium	Child bitten by sibling 6 months prior to his death from AIDS. No baseline HIV test. Tested HIV positive after death of sibling. No other HIV risk factors reported
Anonymous 29	1987	Unknown	Bite (community, intentional)	Yes	Bite to leg	1	Yes	Yes	No	Low	HIV negative 4 years before the bite. HIV positive when tested 2 years post incident. Untraceable sexual partner. Higher risk injury as blood in mouth from teeth being knocked out
Khajotia 27	1997	Columbia	Bite (community, unintentional)	Yes	Mucosa on lip broken by kissing	1	No	Unknown	Unknown	Low	Bite is unlikely route of transmission: the biter was not confirmed to be HIV positive; recipient remained HIV negative at 7 months after bite and seroconverted 10 months after the bite
Andreo et al. 24	2004	Brazil	Bite (during seizure)	Yes	Deep bite (sutured)	1	Yes	Yes	No	Confirmed	Mother bitten by son during a seizure relating to AIDS-defining illness. Seroconversion 27 days later and phylogenetic linkage

*Protagonist presumed viraemic if report is from pre-ART era or protagonist has AIDS-defining or critical illness in the absence of documented ART.
^†Two cases described. Only one description provided original data; the other was a repetition of a case reported elsewhere.
ART, antiretroviral therapy; CDC, Centers for Disease Control and Prevention; HCW, health care worker; ZDV, zidovudine.